Alexander Badyaev

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• Badyaev, A. V. (2013). "Homeostatic hitchhiking": A mechanism for the evolutionary retention of complex adaptations. Integrative and Comparative Biology, 53(6), 913-922.
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  Abstract: The complexity of organismal organization channels and accommodates novel genomic and developmental modifications. Here, I extend this perspective to suggest that emergent processes that dominate homeostasisco-option, re-use, and recombination of accumulated elementscan create configurations and dependencies among these elements that strongly reduce the number of evolutionary steps needed for the evolution of precise novel adaptations. Evolutionary retention and environmental matching of such configurations are further facilitated when they include elements of homeostasis that are responsive to particular environmental cues. I apply this perspective to the study of evolution of sex-biased egg-laying in birds, a phenomenon that combines precision, complexity, context-dependency, and reversibility. I show that homeostatic hitchhiking can overcome the main difficulty in the evolution of this adaptationthe perceived necessity of de novo co-evolution of oogenesis, sex-determination, and order of ovulation in each environmental context something that would require unrealistic expectations of evolutionary rates and population sizes and is not a desirable outcome for a process that needs to retain substantial environmental sensitivity. First, I explain the rationale behind the homeostatic-hitchhiking hypothesis and outline its predictions specifically for studies of sex-bias in order of egg-laying. Second, I show that a combination of self-regulatory and emergent processes and ubiquitous re-use of conserved growth factors make oogenesis particularly amendable to homeostatic hitchhiking. Third, I review empirical evidence for this mechanism in the rapid evolution of adaptive sex-biased order of egg-laying that accompanied colonization of North America by the house finch (Carpodacus mexicanus). © The Author 2013. All rights reserved.
• Badyaev, A., & Badyaev, A. -. (2013). "Homeostatic Hitchhiking": A Mechanism for the Evolutionary Retention of Complex Adaptations. Integrative and comparative biology.
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  The complexity of organismal organization channels and accommodates novel genomic and developmental modifications. Here, I extend this perspective to suggest that emergent processes that dominate homeostasis-co-option, re-use, and recombination of accumulated elements-can create configurations and dependencies among these elements that strongly reduce the number of evolutionary steps needed for the evolution of precise novel adaptations. Evolutionary retention and environmental matching of such configurations are further facilitated when they include elements of homeostasis that are responsive to particular environmental cues. I apply this perspective to the study of evolution of sex-biased egg-laying in birds, a phenomenon that combines precision, complexity, context-dependency, and reversibility. I show that homeostatic hitchhiking can overcome the main difficulty in the evolution of this adaptation-the perceived necessity of de novo co-evolution of oogenesis, sex-determination, and order of ovulation in each environmental context-something that would require unrealistic expectations of evolutionary rates and population sizes and is not a desirable outcome for a process that needs to retain substantial environmental sensitivity. First, I explain the rationale behind the homeostatic-hitchhiking hypothesis and outline its predictions specifically for studies of sex-bias in order of egg-laying. Second, I show that a combination of self-regulatory and emergent processes and ubiquitous re-use of conserved growth factors make oogenesis particularly amendable to homeostatic hitchhiking. Third, I review empirical evidence for this mechanism in the rapid evolution of adaptive sex-biased order of egg-laying that accompanied colonization of North America by the house finch (Carpodacus mexicanus).
• Newman, S. A., Mezentseva, N. V., & Badyaev, A. V. (2013). Gene loss, thermogenesis, and the origin of birds. Annals of the New York Academy of Sciences, 1289(1), 36-47.
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  PMID: 23550607;Abstract: Compared to related taxa, birds have exceptionally enlarged and diversified skeletal muscles, features that are closely associated with skeletal diversification and are commonly explained by a diversity of avian ecological niches and locomotion types. The thermogenic muscle hypothesis (TMH) for the origin of birds proposes that such muscle hyperplasia and the associated skeletal innovations are instead the consequence of the avian clade originating from an ancestral population that underwent several successive episodes of loss of genes associated with thermogenesis, myogenesis, and skeletogenesis. Direct bird ancestors met this challenge with a combination of behavioral strategies (e.g., brooding of nestlings) and acquisition of a variety of adaptations for enhanced nonshivering thermogenesis in skeletal muscle. The latter include specific biochemical alterations promoting muscle heat generation and dramatic expansion of thigh and breast muscle mass. The TMH proposes that such muscle hyperplasia facilitated bipedality, freeing upper limbs for new functions (e.g., flight, swimming), and, by altering the mechanical environment of embryonic development, generated skeletal novelties, sometimes abruptly, that became distinctive features of the avian body plan. © 2013 New York Academy of Sciences.
• Newman, S. A., Mezentseva, N. V., Badyaev, A. V., Mousseau, T., & Fox, C. (2013). Gene loss, thermogenesis, and the origin of birds. YEAR IN EVOLUTIONARY BIOLOGY, 1289, 36-47.
• Badyaev, A., Landeen, E. A., & Badyaev, A. -. (2012). Developmental integration of feather growth and pigmentation and its implications for the evolution of diet-derived coloration. Journal of experimental zoology. Part B, Molecular and developmental evolution, 318(1).
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  Variation in avian coloration is produced by coordinated pigmentation of thousands of growing feathers that vary in shape and size. Although the functional consequences of avian coloration are frequently studied, little is known about its developmental basis, and, specifically, the rules that link feather growth to pigment uptake and synthesis. Here, we combine biochemical, modeling, and morphometric techniques to examine the developmental basis of feather pigmentation in house finches (Carpodacus mexicanus)--a species with extensive variation in both growth dynamics of ornamental feathers and their carotenoid pigmentation. We found that the rate of carotenoid uptake was constant across a wide range of feather sizes and shapes, and the relative pigmented area of feathers was independent of the total amount of deposited carotenoids. Analysis of the developmental linkage of feather growth and pigment uptake showed that the mechanisms behind partitioning the feather into pigmented and nonpigmented parts and the mechanisms regulating carotenoid uptake into growing feathers are partially independent. Carotenoid uptake strongly covaried with early elements of feather differentiation (the barb addition rate and diameter), whereas the pigmented area was most closely associated with the rate of feather growth. We suggest that strong effects of carotenoid uptake on genetically integrated mechanisms of feather growth and differentiation provide a likely route for genetic assimilation of diet-dependent coloration.
• Landeen, E. A., & Badyaev, A. V. (2012). Developmental integration of feather growth and pigmentation and its implications for the evolution of diet-derived coloration. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 318 B(1), 59-70.
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  PMID: 22028247;Abstract: Variation in avian coloration is produced by coordinated pigmentation of thousands of growing feathers that vary in shape and size. Although the functional consequences of avian coloration are frequently studied, little is known about its developmental basis, and, specifically, the rules that link feather growth to pigment uptake and synthesis. Here, we combine biochemical, modeling, and morphometric techniques to examine the developmental basis of feather pigmentation in house finches (Carpodacus mexicanus)-a species with extensive variation in both growth dynamics of ornamental feathers and their carotenoid pigmentation. We found that the rate of carotenoid uptake was constant across a wide range of feather sizes and shapes, and the relative pigmented area of feathers was independent of the total amount of deposited carotenoids. Analysis of the developmental linkage of feather growth and pigment uptake showed that the mechanisms behind partitioning the feather into pigmented and nonpigmented parts and the mechanisms regulating carotenoid uptake into growing feathers are partially independent. Carotenoid uptake strongly covaried with early elements of feather differentiation (the barb addition rate and diameter), whereas the pigmented area was most closely associated with the rate of feather growth. We suggest that strong effects of carotenoid uptake on genetically integrated mechanisms of feather growth and differentiation provide a likely route for genetic assimilation of diet-dependent coloration. © 2011 Wiley Periodicals, Inc..
• Badyaev, A. V. (2011). Origin of the fittest: Link between emergentvariation and evolutionary change as acritical question in evolutionary biology. Proceedings of the Royal Society B: Biological Sciences, 278(1714), 1921-1929.
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  PMID: 21490021;PMCID: PMC3107662;Abstract: In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions inprotein networks and emergent developmental processes can delineate the directions of evolutionarychange, including the opportunity for natural selection. These effects are reflected in the evolution of developmentalprogrammes that link genomic architecture with a corresponding functioning phenotype. Tworecent findings call for closer examination of the rules by which these links are constructed. First is the realizationthat high dimensionality of genotypes and emergent properties of autonomous developmentalprocesses (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypicand genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conservedgene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generativeprocesses. Establishing the causal reciprocal links between ongoing neutral expansion of genomicarchitecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversificationtherefore becomes an important goal of evolutionary biology and is the latest reincarnation of thesearch for a framework that links development, functioning and evolution of phenotypes. Here I examine,in the light of recent empirical advances, two evolutionary concepts that are central to this framework-naturalselection and inheritance-the general rules by which they become associated with emergentdevelopmental and homeostatic processes and the role that they play in descent with modification. © 2011 The Royal Society.
• Badyaev, A. V. (2011). Perspectives in ornithology: How do precise adaptive features arise in development? Examples with evolution of context-specific sex ratios and perfect beaks. Auk, 128(3), 467-474.
• Badyaev, A., & Badyaev, A. -. (2011). Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology. Proceedings. Biological sciences / The Royal Society, 278(1714).
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  In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions in protein networks and emergent developmental processes can delineate the directions of evolutionary change, including the opportunity for natural selection. These effects are reflected in the evolution of developmental programmes that link genomic architecture with a corresponding functioning phenotype. Two recent findings call for closer examination of the rules by which these links are constructed. First is the realization that high dimensionality of genotypes and emergent properties of autonomous developmental processes (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypic and genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conserved gene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generative processes. Establishing the causal reciprocal links between ongoing neutral expansion of genomic architecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversification therefore becomes an important goal of evolutionary biology and is the latest reincarnation of the search for a framework that links development, functioning and evolution of phenotypes. Here I examine, in the light of recent empirical advances, two evolutionary concepts that are central to this framework-natural selection and inheritance-the general rules by which they become associated with emergent developmental and homeostatic processes and the role that they play in descent with modification.
• Stein, L. R., & Badyaev, A. V. (2011). Evolution of eggshell structure during rapid range expansion in a passerine bird. Functional Ecology, 25(6), 1215-1222.
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  Abstract: 1.Environmental factors such as temperature, humidity and partial oxygen pressure can affect avian eggshell structure because gas exchange across the shell must allow sufficient water loss while preventing dehydration of the embryo. Studies of species with known chronology of colonization of novel environments provide a powerful insight into the relative importance of ecological factors shaping the evolution of eggshell structure. 2.Here, we examined changes in eggshell structure that accompanied rapid range expansion of house finches (Carpodacus mexicanus) across North America. We analysed thickness and pore density in eggshells from three ecologically distinct populations: the native desert population in southwestern Arizona and two 30-year-old populations in the northwestern (north-west Montana) and southeastern (south-east Alabama) parts of the species' range. We also conducted cross-foster exchanges of freshly laid eggs within and between the northwestern and southeastern populations to examine consequences of population differences in eggshell structure on embryo development. 3.Eggshell structure was most distinct in a recently established population inhabiting higher humidity environment (southeastern Alabama), where eggs were the largest, eggshells the thickest and pore density the lowest. Populations that experienced highly distinct ambient temperatures (southwestern Arizona and northwestern Montana) nevertheless had similar eggshell structure. These results were corroborated by experiments where humidity differences between cross-fostered nests had twice the effect on embryo survival compared to the effect of change in ambient temperature. Correspondingly, experimental egg exchanges between southeastern. Alabama and northwestern Montana populations were associated with fourfold increase in embryo mortality compared to within-population egg exchanges. 4.We document rapid evolution of eggshell structure in response to colonization of novel environments and establish the relative importance of environmental factors on avian eggshells. We discuss these results in relation to population variation in incubation behaviour and its ability to shield eggshell structure from the selection exerted by novel environments. © 2011 The Authors. Functional Ecology © 2011 British Ecological Society.
• Badyaev, A. V. (2010). The beak of the other finch: Coevolution of genetic covariance structure and developmental modularity during adaptive evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1543), 1111-1126.
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  PMID: 20194173;PMCID: PMC2830233;Abstract: The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak's precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies-a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis-beak depth-was mirrored in the structure of beak's additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution. © 2010 The Royal Society.
• Badyaev, A., & Badyaev, A. -. (2010). The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 365(1543).
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  The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak's precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies-a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis-beak depth-was mirrored in the structure of beak's additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.
• Badyaev, A., Oh, K. P., & Badyaev, A. -. (2010). Structure of social networks in a passerine bird: consequences for sexual selection and the evolution of mating strategies. The American naturalist, 176(3).
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  The social environment is a critical determinant of fitness and, in many taxa, is shaped by an individual's behavioral discrimination among social contexts, suggesting that animals can actively influence the selection they experience. In competition to attract females, males may modify sexual selection by choosing social environments in which they are more attractive relative to rivals. Across the population, such behaviors should influence sexual selection patterns by altering the relationship between male mating success and sexual ornament elaboration. Here we use network analysis to examine patterns of male social behavior in relation to plumage ornamentation and mating success in a free-living population of house finches. During the nonbreeding season, less elaborate males changed associations with distinct social groups more frequently, compared to more elaborate males that showed greater fidelity to a single social group. By the onset of pair formation, socially labile males effectively increased their attractiveness relative to other males in the same flocks. Consequently, males that frequently moved between social groups had greater pairing success than less social individuals with equivalent sexual ornamentation. We discuss these results in relation to conditional mating tactics and the role of social behavior in evolutionary change by sexual selection.
• Badyaev, A., Young, R. L., & Badyaev, A. -. (2010). Developmental plasticity links local adaptation and evolutionary diversification in foraging morphology. Journal of experimental zoology. Part B, Molecular and developmental evolution, 314(6).
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  Developmental plasticity is thought to reconcile the constraining role of natural selection in maintaining local adaptation with evolutionary diversification under novel conditions, but empirical documentations are rare. In vertebrates, growth and development of bones is partially guided by contractions of attached musculature and such muscle activity changes progressively through embryonic development from sporadic motility to direct functional effects. In species with short generation times, delayed skull maturation extends the guiding effects of muscle activity on formation of foraging morphology into adulthood, providing an opportunity to directly examine the links between plasticity of bone development, ecological adaptations, and evolutionary diversification in foraging morphology. In this case, the morphological consequences of inputs due to local functional requirements should be evident in adaptive divergence across taxa. Here we provide evidence that epigenetic regulation of bone growth in Soricid shrews may enable both development of local adaptations and evolutionary divergence in mandibular morphology. We contrast the effects of muscle stimulation on early- vs. late-maturing components of, foraging apparatus to show that the morphology of late-maturing components is more affected by functional requirements than are early-ossifying traits. Further, the divergence in foraging morphology across shrew species occurs along the directions delineated by inductive effects of muscle loading and bite force on bone formation in late-maturing but not early-maturing mandible components within species. These results support the hypothesis that developmental plasticity can link maintenance of local adaptations with evolutionary diversification in morphology.
• Oh, K. P., & Badyaev, A. V. (2010). Structure of social networks in a passerine bird: Consequences for sexual selection and the evolution of mating strategies. American Naturalist, 176(3), E80-E89.
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  PMID: 20608873;Abstract: The social environment is a critical determinant of fitness and, in many taxa, is shaped by an individual's behavioral discrimination among social contexts, suggesting that animals can actively influence the selection they experience. In competition to attract females, males may modify sexual selection by choosing social environments in which they are more attractive relative to rivals. Across the population, such behaviors should influence sexual selection patterns by altering the relationship between male mating success and sexual ornament elaboration. Here we use network analysis to examine patterns of male social behavior in relation to plumage ornamentation and mating success in a free-living population of house finches. During the nonbreeding season, less elaborate males changed associations with distinct social groups more frequently, compared to more elaborate males that showed greater fidelity to a single social group. By the onset of pair formation, socially labile males effectively increased their attractiveness relative to other males in the same flocks. Consequently, males that frequently moved between social groups had greater pairing success than less social individuals with equivalent sexual ornamentation. We discuss these results in relation to conditional mating tactics and the role of social behavior in evolutionary change by sexual selection. © 2010 by The University of Chicago.
• Stein, L. R., Oh, K. P., & Badyaev, A. V. (2010). Fitness consequences of male provisioning of incubating females in a desert passerine bird. Journal of Ornithology, 151(1), 227-233.
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  Abstract: Male provisioning of incubating females can increase reproductive success by maintaining physiological condition of females and consistency of incubation. The effects of male provisioning on the maintenance of incubation temperature and embryo development should be particularly pronounced in environments where ambient temperature exceeds the tolerance of unincubated eggs and where consistency of female incubation might be particularly important for hatching success. Here, we investigated the reproductive consequences of incubation feeding in a desert population of House Finches (Carpodacus mexicanus) in southwestern Arizona. We found that greater nest attentiveness by females was related to higher minimum incubation nest temperature, that in turn was closely associated with hatching success. Only 44% of males regularly provisioned their incubating females. Although provisioned females maintained higher incubation temperature and took fewer incubation breaks than non-provisioned females, overall, male provisioning did not influence incubation dynamics or hatching success. Further, a male's incubation feeding rate did not correlate with male provisioning of nestlings. These results corroborate the finding that, in male House Finches, neither provisioning of incubating females nor pre-incubation courtship feeding are associated with increases in circulating pituitary prolactin--the hormone regulating male provisioning of nestlings. We suggest that incubation provisioning by male might be a component of pair maintenance behavior and that variation in male incubation behavior is best understood in relation to asymmetries in residual reproductive values between the mates. © Dt. Ornithologen-Gesellschaft e.V. 2009.
• Young, R. L., & Badyaev, A. V. (2010). Developmental plasticity links local adaptation and evolutionary diversification in foraging morphology. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314 B(6), 434-444.
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  PMID: 20700888;Abstract: Developmental plasticity is thought to reconcile the constraining role of natural selection in maintaining local adaptation with evolutionary diversification under novel conditions, but empirical documentations are rare. In vertebrates, growth and development of bones is partially guided by contractions of attached musculature and such muscle activity changes progressively through embryonic development from sporadic motility to direct functional effects. In species with short generation times, delayed skull maturation extends the guiding effects of muscle activity on formation of foraging morphology into adulthood, providing an opportunity to directly examine the links between plasticity of bone development, ecological adaptations, and evolutionary diversification in foraging morphology. In this case, the morphological consequences of inputs due to local functional requirements should be evident in adaptive divergence across taxa. Here we provide evidence that epigenetic regulation of bone growth in Soricid shrews may enable both development of local adaptations and evolutionary divergence in mandibular morphology. We contrast the effects of muscle stimulation on early- vs. late-maturing components of, foraging apparatus to show that the morphology of late-maturing components is more affected by functional requirements than are early-ossifying traits. Further, the divergence in foraging morphology across shrew species occurs along the directions delineated by inductive effects of muscle loading and bite force on bone formation in late-maturing but not early-maturing mandible components within species. These results support the hypothesis that developmental plasticity can link maintenance of local adaptations with evolutionary diversification in morphology. © 2010 Wiley-Liss, Inc.
• Young, R. L., Sweeney, M. J., & Badyaev, A. V. (2010). Morphological diversity and ecological similarity: versatility of muscular and skeletal morphologies enables ecological convergence in shrews. Functional Ecology, 24(3), 556-565.
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  Abstract: Summary: 1. Ecological convergence in morphology among taxa of distinct evolutionary histories is a common illustration of the efficacy of natural selection. Ecological convergence is often enabled by functional redundancy of complex morphological structures, such that modification of existing morphologies in response to similar functional requirements can lead to the development and evolution of morphological diversity. Thus, studies of the mechanisms that enable the development of similar adaptations in taxa with distinct morphologies provide important insights into both the evolution of past adaptations and patterns of future evolutionary divergence. 2. Here, we examine mechanisms that have enabled ecological convergence in foraging morphology among four geographically isolated and morphologically distinct populations of shrews: south-eastern Arizona and north-central New Mexico populations of the montane shrews (Sorex monticolus) and northern California and north-central Montana populations of the vagrant shrew (S. vagrans). 3. We show that despite overlap in diet, populations had distinct skeletal and muscular morphologies of the mandible. This association between ecological convergence and morphological uniqueness among populations was enabled by versatility of foraging morphologies that generated similar functional outputs. 4. In addition, we found that populations exhibited unique skeletal and muscular correlations with diet suggesting that distinct muscular and morphological components of the complex foraging apparatus can be used for a particular resource. This result corroborates a previous finding that extensive modularity in mandibular development allows diverse morphologies to generate equivalent functions and utilize similar resources across taxa. 5. Synthesis. We conclude that the observed functional and ecological convergences resulted from population-specific musculoskeletal interactions, and suggest that the differences in skeletal and muscular morphologies observed among these populations reflect evolved differences in plasticity of the skeletal and muscular components of the mandible. © 2009 The Authors. Journal compilation © 2009 British Ecological Society.
• Badyaev, A. V. (2009). Evolutionary significance of phenotypic accommodation in novel environments: An empirical test of the Baldwin effect. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1520), 1125-1141.
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  PMID: 19324617;PMCID: PMC2666683;Abstract: When faced with changing environments, organisms rapidly mount physiological and behavioural responses, accommodating new environmental inputs in their functioning. The ubiquity of this process contrasts with our ignorance of its evolutionary significance: whereas within-generation accommodation of novel external inputs has clear fitness consequences, current evolutionary theory cannot easily link functional importance and inheritance of novel accommodations. One hundred and twelve years ago, J. M. Baldwin, H. F. Osborn and C. L. Morgan proposed a process (later termed the Baldwin effect) by which non-heritable developmental accommodation of novel inputs, which makes an organism fit in its current environment, can become internalized in a lineage and affect the course of evolution. The defining features of this process are initial overproduction of random (with respect to fitness) developmental variation, followed by within-generation accommodation of a subset of this variation by developmental or functional systems ('organic selection'), ensuring the organism's fit and survival. Subsequent natural selection sorts among resultant developmental variants, which, if recurrent and consistently favoured, can be inherited when existing genetic variance includes developmental components of individual modifications or when the ability to accommodate novel inputs is itself heritable. Here, I show that this process is consistent with the origin of novel adaptations during colonization of North America by the house finch. The induction of developmental variation by novel environments of this species's expanding range was followed by homeostatic channelling, phenotypic accommodation and directional cross-generational transfer of a subset of induced developmental outcomes favoured by natural selection. These results emphasize three principal points. First, contemporary novel adaptations result mostly from reorganization of existing structures that shape newly expressed variation, giving natural selection an appearance of a creative force. Second, evolutionary innovations and maintenance of adaptations are different processes. Third, both the Baldwin and parental effects are probably a transient state in an evolutionary cycle connecting initial phenotypic retention of adaptive changes and their eventual genetic determination and, thus, the origin of adaptation and evolutionary change. © 2009 The Royal Society.
• Badyaev, A. V., & Uller, T. (2009). Parental effects in ecology and evolution: Mechanisms, processes and implications. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1520), 1169-1177.
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  PMID: 19324619;PMCID: PMC2666689;Abstract: As is the case with any metaphor, parental effects mean different things to different biologists - from developmental induction of novel phenotypic variation to an evolved adaptation, and from epigenetic transference of essential developmental resources to a stage of inheritance and ecological succession. Such a diversity of perspectives illustrates the composite nature of parental effects that, depending on the stage of their expression and whether they are considered a pattern or a process, combine the elements of developmental induction, homeostasis, natural selection, epigenetic inheritance and historical persistence. Here, we suggest that by emphasizing the complexity of causes and influences in developmental systems and by making explicit the links between development, natural selection and inheritance, the study of parental effects enables deeper understanding of developmental dynamics of life cycles and provides a unique opportunity to explicitly integrate development and evolution. We highlight these perspectives by placing parental effects in a wider evolutionary framework and suggest that far from being only an evolved static outcome of natural selection, a distinct channel of transmission between parents and offspring, or a statistical abstraction, parental effects on development enable evolution by natural selection by reliably transferring developmental resources needed to reconstruct, maintain and modify genetically inherited components of the phenotype. The view of parental effects as an essential and dynamic part of an evolutionary continuum unifies mechanisms behind the origination, modification and historical persistence of organismal form and function, and thus brings us closer to a more realistic understanding of life's complexity and diversity. © 2009 The Royal Society.
• Badyaev, A., & Badyaev, A. -. (2009). Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 364(1520).
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  When faced with changing environments, organisms rapidly mount physiological and behavioural responses, accommodating new environmental inputs in their functioning. The ubiquity of this process contrasts with our ignorance of its evolutionary significance: whereas within-generation accommodation of novel external inputs has clear fitness consequences, current evolutionary theory cannot easily link functional importance and inheritance of novel accommodations. One hundred and twelve years ago, J. M. Baldwin, H. F. Osborn and C. L. Morgan proposed a process (later termed the Baldwin effect) by which non-heritable developmental accommodation of novel inputs, which makes an organism fit in its current environment, can become internalized in a lineage and affect the course of evolution. The defining features of this process are initial overproduction of random (with respect to fitness) developmental variation, followed by within-generation accommodation of a subset of this variation by developmental or functional systems ('organic selection'), ensuring the organism's fit and survival. Subsequent natural selection sorts among resultant developmental variants, which, if recurrent and consistently favoured, can be inherited when existing genetic variance includes developmental components of individual modifications or when the ability to accommodate novel inputs is itself heritable. Here, I show that this process is consistent with the origin of novel adaptations during colonization of North America by the house finch. The induction of developmental variation by novel environments of this species's expanding range was followed by homeostatic channelling, phenotypic accommodation and directional cross-generational transfer of a subset of induced developmental outcomes favoured by natural selection. These results emphasize three principal points. First, contemporary novel adaptations result mostly from reorganization of existing structures that shape newly expressed variation, giving natural selection an appearance of a creative force. Second, evolutionary innovations and maintenance of adaptations are different processes. Third, both the Baldwin and parental effects are probably a transient state in an evolutionary cycle connecting initial phenotypic retention of adaptive changes and their eventual genetic determination and, thus, the origin of adaptation and evolutionary change.
• Badyaev, A., Oh, K. P., & Badyaev, A. -. (2009). Isolation and characterization of 17 microsatellite loci for the house finch (Carpodacus mexicanus). Molecular ecology resources, 9(3).
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  The house finch (Carpodacus mexicanus) has emerged recently as a model species in studies of sexual selection, reproductive physiology, population genetics, and epizootic disease ecology. Here we describe 17 highly polymorphic microsatellite loci for this species. In a sample of 36 individuals, we observed an average of 16 alleles per locus and heterozygosity ranged from 0.61 to 0.97. One locus showed significant deviation from Hardy-Weinberg proportions, but no significant gametic disequilibrium was observed among any of the loci. Amplification by polymerase chain reaction was optimized under similar parameters across loci, thereby facilitating multiplexing and rapid multilocus genotyping.
• Badyaev, A., Uller, T., & Badyaev, A. -. (2009). Evolution of "determinants" in sex-determination: a novel hypothesis for the origin of environmental contingencies in avian sex-bias. Seminars in cell & developmental biology, 20(3).
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  Sex-determination is commonly categorized as either "genetic" or "environmental"-a classification that obscures the origin of this dichotomy and the evolution of sex-determining factors. The current focus on static outcomes of sex-determination provides little insight into the dynamic developmental processes by which some mechanisms acquire the role of sex determinants. Systems that combine "genetic" pathways of sex-determination (i.e., sex chromosomes) with "environmental" pathways (e.g., epigenetically induced segregation distortion) provide an opportunity to examine the evolutionary relationships between the two classes of processes and, ultimately, illuminate the evolution of sex-determining systems. Taxa with sex chromosomes typically undergo an evolutionary reduction in size of one of the sex chromosomes due to suppressed recombination, resulting in pronounced dimorphism of the sex chromosomes, and setting the stage for emergence of epigenetic compensatory mechanisms regulating meiotic segregation of heteromorphic sex chromosomes. Here we propose that these dispersed and redundant regulatory mechanisms enable environmental contingency in genetic sex-determination in birds and account for frequently documented context-dependence in avian sex-determination. We examine the evolution of directionality in such sex-determination as a result of exposure of epigenetic regulators of meiosis to natural selection and identify a central role of hormones in integrating female reproductive homeostasis, resource allocation to oocytes, and offspring sex. This approach clarifies the evolutionary relationship between sex-specific molecular genetic mechanisms of sex-determination and non-sex-specific epigenetic regulators of meiosis and demonstrates that both can determine sex. Our perspective shows how non-sex-specific mechanisms can acquire sex-determining function and, by establishing the explicit link between physiological integration of oogenesis and sex-determination, opens new avenues to the studies of adaptive sex-bias and sex-specific resource allocation in species with genetic sex-determination.
• Hamstra, T. L., & Badyaev, A. V. (2009). Comprehensive investigation of ectoparasite community and abundance across life history stages of avian host. Journal of Zoology, 278(2), 91-99.
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  Abstract: Fitness consequences of ectoparasitism are expressed over the lifetime of their hosts in relation to variation in composition and abundance of the entire ectoparasite community and across all host life history stages. However, most empirical studies have focused on parasite species-specific effects and only during some life history stages. We conducted a systematic, year-long survey of an ectoparasite community in a wild population of house finches Carpodacus mexicanus Müller in south-western Arizona, with a specific focus on ecological and behavioral correlates of ectoparasite prevalence and abundance. We investigated five ectoparasite species: two feather mite genera - both novel for house finches - Strelkoviacarus (Analgidae) and Dermoglyphus (Dermoglyphidae), the nest mite Pellonyssus reedi (Macronyssidae), and the lice Menacanthus alaudae (Menoponidae) and Ricinus microcephalus (Ricinidae). Mite P. reedi and louse Menacanthus alaudae abundance peaked during host breeding season, especially in older birds, whereas feather mite abundance peaked during molt. Overall, breeding birds had more P. reedi than non-breeders, molting males had greater abundance of feather mites than molting females and non-molting males, and young males had more feather mites than older males. We discuss these results in relation to natural history of ectoparasites under study and suggest that ectoparasites might synchronize their life cycles to those of their hosts. Pronounced differences in relative abundance of ectoparasite species among host's life history stages have important implications for evolution of parasite-specific host defenses. © 2009 The Zoological Society of London.
• Mousseau, T. A., Uller, T., Wapstra, E., & Badyaev, A. V. (2009). Evolution of maternal effects: Past and present. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1520), 1035-1038.
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  PMID: 19324608;PMCID: PMC2666690;
• Oh, K. P., & Badyaev, A. V. (2009). Isolation and characterization of 17 microsatellite loci for the house finch (Carpodacus mexicanus). Molecular Ecology Resources, 9(3), 1029-1031.
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  PMID: 21564828;Abstract: The house finch (Carpodacus mexicanus) has emerged recently as a model species in studies of sexual selection, reproductive physiology, population genetics, and epizootic disease ecology. Here we describe 17 highly polymorphic microsatellite loci for this species. In a sample of 36 individuals, we observed an average of 16 alleles per locus and heterozygosity ranged from 0.61 to 0.97. One locus showed significant deviation from Hardy-Weinberg proportions, but no significant gametic disequilibrium was observed among any of the loci. Amplification by polymerase chain reaction was optimized under similar parameters across loci, thereby facilitating multiplexing and rapid multilocus genotyping. © 2009 Blackwell Publishing Ltd.
• Uller, T., & Badyaev, A. V. (2009). Evolution of "determinants" in sex-determination: A novel hypothesis for the origin of environmental contingencies in avian sex-bias. Seminars in Cell and Developmental Biology, 20(3), 304-312.
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  PMID: 19073270;Abstract: Sex-determination is commonly categorized as either "genetic" or "environmental"-a classification that obscures the origin of this dichotomy and the evolution of sex-determining factors. The current focus on static outcomes of sex-determination provides little insight into the dynamic developmental processes by which some mechanisms acquire the role of sex determinants. Systems that combine "genetic" pathways of sex-determination (i.e., sex chromosomes) with "environmental" pathways (e.g., epigenetically induced segregation distortion) provide an opportunity to examine the evolutionary relationships between the two classes of processes and, ultimately, illuminate the evolution of sex-determining systems. Taxa with sex chromosomes typically undergo an evolutionary reduction in size of one of the sex chromosomes due to suppressed recombination, resulting in pronounced dimorphism of the sex chromosomes, and setting the stage for emergence of epigenetic compensatory mechanisms regulating meiotic segregation of heteromorphic sex chromosomes. Here we propose that these dispersed and redundant regulatory mechanisms enable environmental contingency in genetic sex-determination in birds and account for frequently documented context-dependence in avian sex-determination. We examine the evolution of directionality in such sex-determination as a result of exposure of epigenetic regulators of meiosis to natural selection and identify a central role of hormones in integrating female reproductive homeostasis, resource allocation to oocytes, and offspring sex. This approach clarifies the evolutionary relationship between sex-specific molecular genetic mechanisms of sex-determination and non-sex-specific epigenetic regulators of meiosis and demonstrates that both can determine sex. Our perspective shows how non-sex-specific mechanisms can acquire sex-determining function and, by establishing the explicit link between physiological integration of oogenesis and sex-determination, opens new avenues to the studies of adaptive sex-bias and sex-specific resource allocation in species with genetic sex-determination. © 2008 Elsevier Ltd. All rights reserved.
• Badyaev, A. V. (2008). Maternal effects as generators of evolutionary change: A reassessment. Annals of the New York Academy of Sciences, 1133, 151-161.
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  PMID: 18559819;Abstract: Despite being a center of debate in biology for centuries, the connection between the generation of novel adaptive variation and its inheritance remains a contentious issue. In evolutionary and behavioral ecology, assigning natural and sexual selection a creative and anticipatory role unmasks the need to explicitly consider the link between a trait's functional importance and its inheritance and results in confusion about selection as an adaptive modifier of development versus selection as a passive filter of already produced forms. In developmental genetics, an emphasis on regulatory versus coding aspects of molecular evolutionary change overlooks the fundamental question of the origination of an inherited developmental toolkit and assignment of its regulatory functions. Because maternal effects, by definition, combine developmental induction of functionally important changes and their inheritance, they bridge the origin and evolution of organismal adaptability, at least on short time scales. The explosion of empirical studies of maternal effects raises a question - are maternal effects ubiquitous but short-term adjusters and fine-tuners of an evolved form with only secondary importance for evolutionary change? Or are they a particularly clear example of a stage in a continuum of inheritance systems that accumulates, internalizes, and passes on the most consistent and adaptive organism-environment interactions? Here I place recent empirical studies of avian maternal effects into the evolutionary framework of variation, selection, and inheritance to examine whether maternal effects provide a window into evolutionary processes. © 2008 New York Academy of Sciences.
• Badyaev, A. V., & Oh, K. P. (2008). Environmental induction and phenotypic retention of adaptive maternal effects. BMC Evolutionary Biology, 8(1).
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  PMID: 18182118;PMCID: PMC2231342;Abstract: Background. The origin of complex adaptations is one of the most controversial questions in biology. Environmental induction of novel phenotypes, where phenotypic retention of adaptive developmental variation is enabled by organismal complexity and homeostasis, can be a starting point in the evolution of some adaptations, but empirical examples are rare. Comparisons of populations that differ in historical recurrence of environmental induction can offer insight into its evolutionary significance, and recent colonization of North America by the house finch (Carpodacus mexicanus) provides such an opportunity. Results. In both native (southern Arizona) and newly established (northern Montana, 18 generations) populations, breeding female finches exhibit the same complex adaptation - a sex-bias in ovulation sequence - in response to population-specific environmental stimulus of differing recurrence. We document that, in the new population, the adaptation is induced by a novel environment during females' first breeding and is subsequently retained across breeding attempts. In the native population, first-breeding females expressed a precise adaptive response to a recurrent environmental stimulus without environmental induction. We document strong selection on environmental cue recognition in both populations and find that rearrangement of the same proximate mechanism - clustering of oocytes that become males and females - can enable an adaptive response to distinct environmental stimuli. Conclusion. The results show that developmental plasticity induced by novel environmental conditions confers significant fitness advantages to both maternal and offspring generations and might play an important role not only in the successful establishment of this invasive species across the widest ecological range of extant birds, but also can link environmental induction and genetic inheritance in the evolution of novel adaptations. © 2008 Badyaev and Oh; licensee BioMed Central Ltd.
• Badyaev, A. V., Young, R. L., Hill, G. E., & Duckworth, R. A. (2008). Evolution of sex-biased maternal effects in birds. IV. Intra-ovarian growth dynamics can link sex determination and sex-specific acquisition of resources. Journal of Evolutionary Biology, 21(2), 449-460.
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  PMID: 18205775;Abstract: The evolutionary importance of maternal effects is determined by the interplay of maternal adaptations and strategies, offspring susceptibility to these strategies, and the similarity of selection pressures between the two generations. Interaction among these components, especially in species where males and females differ in the costs and requirements of growth, limits inference about the evolution of maternal strategies from their expression in the offspring phenotype alone. As an alternative approach, we examine divergence in the proximate mechanisms underlying maternal effects across three house finch populations with contrasting patterns of sex allocation: an ancestral population that shows no sex-biased ovulation, and two recently established populations at the northern and southern boundaries of the species range that have opposite sequences of ovulation of male and female eggs. For each population, we examined how oocyte acquisition of hormones, carotenoids and vitamins was affected by oocyte growth and overlap with the same and opposite sexes. Our results suggest that sex-specific acquisition of maternal resources and sex determination of oocytes are linked in this system. We report that acquisition of testosterone by oocytes that become males was not related to growth duration, but instead covaried with temporal exposure to steroids and overlap with other male oocytes. In female oocytes, testosterone acquisition increased with the duration of growth and overlap with male oocytes, but decreased with overlap with female oocytes. By contrast, acquisition of carotenoids and vitamins was mostly determined by organism-wide partitioning among oocytes and oocyte-specific patterns of testosterone accumulation, and these effects did not differ between the sexes. These results provide important insights into three unresolved phenomena in the evolution of maternal effects - (i) the evolution of sex-specific maternal allocation in species with simultaneously developing neonates of both sexes; (ii) the link between sex determination and sex-specific acquisition of maternal products; and (iii) the evolution of context-dependent modulation of maternal effects. © 2008 The Authors.
• Badyaev, A. V., Young, R. L., Oh, K. P., & Addison, C. (2008). Evolution on a local scale: Developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats. Evolution, 62(8), 1951-1964.
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  PMID: 18507745;Abstract: Divergent selection on traits involved in both local adaptation and the production of mating signals can strongly facilitate population differentiation. Because of its links to foraging morphologies and cultural inheritance song of birds can contribute particularly strongly to maintenance of local adaptations. In two adjacent habitats - native Sonoran desert and urban areas - house finches (Carpodacus mexicanus) forage on seeds that are highly distinct in size and shell hardness and require different bite forces and bill morphologies. Here, we first document strong and habitat-specific natural selection on bill traits linked to bite force and find adaptive modifications of bite force and bill morphology and associated divergence in courtship song between the two habitats. Second, we investigate the developmental basis of this divergence and find that early ontogenetic tissue transformation in bill, but not skeletal traits, is accelerated in the urban population and that the mandibular primordia of the large-beaked urban finches express bone morphogenetic proteins (BMP) earlier and at higher level than those of the desert finches. Further, we show that despite being geographically adjacent, urban and desert populations are nevertheless genetically distinct corroborating findings of early developmental divergence between them. Taken together, these results suggest that divergent selection on function and development of traits involved in production of mating signals, in combination with localized learning of such signals, can be very effective at maintaining local adaptations, even at small spatial scales and in highly mobile animals. © 2008 The Author(s).
• Badyaev, A., & Badyaev, A. -. (2008). Maternal effects as generators of evolutionary change: a reassessment. Annals of the New York Academy of Sciences, 1133.
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  Despite being a center of debate in biology for centuries, the connection between the generation of novel adaptive variation and its inheritance remains a contentious issue. In evolutionary and behavioral ecology, assigning natural and sexual selection a creative and anticipatory role unmasks the need to explicitly consider the link between a trait's functional importance and its inheritance and results in confusion about selection as an adaptive modifier of development versus selection as a passive filter of already produced forms. In developmental genetics, an emphasis on regulatory versus coding aspects of molecular evolutionary change overlooks the fundamental question of the origination of an inherited developmental toolkit and assignment of its regulatory functions. Because maternal effects, by definition, combine developmental induction of functionally important changes and their inheritance, they bridge the origin and evolution of organismal adaptability, at least on short time scales. The explosion of empirical studies of maternal effects raises a question--are maternal effects ubiquitous but short-term adjusters and fine-tuners of an evolved form with only secondary importance for evolutionary change? Or are they a particularly clear example of a stage in a continuum of inheritance systems that accumulates, internalizes, and passes on the most consistent and adaptive organism-environment interactions? Here I place recent empirical studies of avian maternal effects into the evolutionary framework of variation, selection, and inheritance to examine whether maternal effects provide a window into evolutionary processes.
• Badyaev, A., Rutkowska, J., & Badyaev, A. -. (2008). Review. Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 363(1497).
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  Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.
• Badyaev, A., Snell-Rood, E. C., & Badyaev, A. -. (2008). Ecological gradient of sexual selection: elevation and song elaboration in finches. Oecologia, 157(3).
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  Ecological gradients in natural and sexual selection often result in evolutionary diversification of morphological, life history, and behavioral traits. In particular, elevational changes in habitat structure and climate not only covary with intensity of sexual selection in many taxa, but may also influence evolution of mating signals. Here we examined variation in courtship song in relation to elevation of breeding across cardueline finches-a subfamily of birds that occupies the widest elevational range of extant birds and shows extensive variation in life histories and sexual selection along this range. We predicted that decrease in sexual selection intensity with elevation of breeding documented in this clade would result in a corresponding evolutionary reduction in elaboration of courtship songs. We controlled for the effects of phylogeny, morphology, and habitat structure to uncover a predicted elevational decline in courtship song elaboration; species breeding at lower elevations sang more elaborated and louder songs compared to their sister species breeding at higher elevations. In addition, lower elevation species had longer songs with more notes, whereas frequency components of song did not vary with elevation. We suggest that changes in sexual selection account for the observed patterns of song variation and discuss how elevational gradient in sexual selection may facilitate divergence in mating signals potentially reinforcing or promoting speciation.
• Oh, K. P., & Badyaev, A. V. (2008). Evolution of adaptation and mate choice: Parental relatedness affects expression of phenotypic variance in a natural population. Evolutionary Biology, 35(2), 111-124.
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  Abstract: Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism's sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure. © Springer Science+Business Media, LLC 2008.
• Rutkowska, J., & Badyaev, A. V. (2008). Meiotic drive and sex determination: Molecular and cytological mechanisms of sex ratio adjustment in birds. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1497), 1675-1686.
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  PMID: 18048292;PMCID: PMC2606724;Abstract: Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species. © 2007 The Royal Society.
• Snell-Rood, E. C., & Badyaev, A. V. (2008). Ecological gradient of sexual selection: Elevation and song elaboration in finches. Oecologia, 157(3), 545-551.
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  PMID: 18607634;Abstract: Ecological gradients in natural and sexual selection often result in evolutionary diversification of morphological, life history, and behavioral traits. In particular, elevational changes in habitat structure and climate not only covary with intensity of sexual selection in many taxa, but may also influence evolution of mating signals. Here we examined variation in courtship song in relation to elevation of breeding across cardueline finches-a subfamily of birds that occupies the widest elevational range of extant birds and shows extensive variation in life histories and sexual selection along this range. We predicted that decrease in sexual selection intensity with elevation of breeding documented in this clade would result in a corresponding evolutionary reduction in elaboration of courtship songs. We controlled for the effects of phylogeny, morphology, and habitat structure to uncover a predicted elevational decline in courtship song elaboration; species breeding at lower elevations sang more elaborated and louder songs compared to their sister species breeding at higher elevations. In addition, lower elevation species had longer songs with more notes, whereas frequency components of song did not vary with elevation. We suggest that changes in sexual selection account for the observed patterns of song variation and discuss how elevational gradient in sexual selection may facilitate divergence in mating signals potentially reinforcing or promoting speciation. © 2008 Springer-Verlag.
• Badyaev, A. V. (2007). Evolvability and robustness in color displays: Bridging the gap between theory and Data. Evolutionary Biology, 34(1-2), 61-71.
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  Abstract: Evolution of diet-derived sexual ornaments-some of the most spectacular and diverse traits in the living world-highlights the gap between modern evolutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Specifically, current theory offers little insight into how strong environmental contingency of diet-dependent color biosynthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an association between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology-how to connect causes of within-generation developmental variation with causes of among-generation and among-taxa variation and thus with causes of evolution? © Springer Science+Business Media, LLC 2007.
• Badyaev, A. V., & Landeen, E. A. (2007). Developmental evolution of sexual ornamentation: Model and a test of feather growth and pigmentation. Integrative and Comparative Biology, 47(2), 221-233.
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  PMID: 21672833;Abstract: A tremendous diversity of avian color displays has stimulated numerous studies of natural and sexual selection. Yet, the developmental mechanisms that produce such diversification, and thus the proximate targets of selection pressures, are rarely addressed and poorly understood. In particular, because feathers are colored during growth, the dynamics of feather growth play a deterministic role in the variation in ornamentation. No study to date, however, has addressed the contribution of feather growth to the expression of carotenoid-based ornamentation. Here, we examine the developmental basis of variation in ornamental feather shapes in male house finches (Carpodacus mexicanus) - a species in which carotenoid displays are under strong natural and sexual selection. First, we use geometric morphometrics to partition the observed shape variation in fully grown feathers among populations, ages, degrees of elaboration, ornamental body parts, and individuals. Second, we use a biologically informed mathematical model of feather growth to predict variation in shape of ornamental feathers due to simulated growth rate, angle of helical growth of feather barbs, initial number of barb ridges, rate of addition of new barbs, barb diameter, and ramus-expansion angle. We find close concordance between among-individual variation in feather shape and hue of entire ornament, and show that this concordance can be attributed to a shared mechanism - growth rate of feather barbs. Predicted differences in feather shape due to rate of addition of barbs and helical angle of feather growth explained observed variation in ornamental area both among individuals and between populations, whereas differences in helical angle of growth and the number of barbs in the feather follicle explained differences in feather shape between ornamental parts and among males of different ages. The findings of a close association of feather growth dynamics and overall ornamentation identify the proximate targets of selection for elaboration of sexual displays. Moreover, the close association of feather growth and pigmentation not only can reinforce condition-dependence in color displays, but can also enable phenotypic and genetic accommodation of novel pigments into plumage displays providing a mechanism for the observed concordance of within-population developmental processes and between-population diversification of color displays.
• Badyaev, A. V., & Vleck, C. M. (2007). Context-dependent development of sexual ornamentation: Implications for a trade-off between current and future breeding efforts. Journal of Evolutionary Biology, 20(4), 1277-1287.
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  PMID: 17584223;Abstract: Allocation of resources into the development of sexual displays is determined by a trade-off between the competing demands of current reproduction and self-maintenance. When reproduction overlaps with acquisition of sexual ornamentation, such as in birds with a yearly post-breeding moult, such a trade-off can be expressed in elaboration of sexual traits used in subsequent matings. In turn, selection for elaboration of sexual ornaments should favour resolution of this trade-off through a modification of the ornaments' development, resulting in variable and life history-dependent development of sexual displays. Here we examined a novel hypothesis that the trade-off between current reproduction and development of sexual ornamentation in the house finch (Carpodacus mexicanus) can be mediated by the shared effects of prolactin - a pituitary hormone that regulates both parental care and moult in this species. We compared developmental variation in sexual ornamentation between breeding, nonbreeding, and juvenile males and examined the relative contribution of residual levels of prolactin and individual condition during moult to the acquisition of sexual ornamentation. Males that invested heavily in parental care entered post-breeding moult in lower condition and later in the season, but their higher plasma prolactin was associated with shorter and more intense moult ultimately resulting in equal or greater elaboration of sexual ornamentation compared with nonparental males. Elaboration of sexual ornamentation of nonparental males that entered moult in greater condition, but with lower prolactin, was produced by longer and earlier moult and by lesser overlap in moult between sexual ornaments. Ornamentation of juvenile males that acquire sexual ornamentation for the first time was closely associated with physiological condition during moult. We discuss the implications of such context-dependent ontogenies of sexual ornamentation and resulting differences in condition-dependence of sexual traits across life history stages on the evolution of female preference for elaborated sexual displays. © 2007 The Authors.
• Badyaev, A., Young, R. L., & Badyaev, A. -. (2007). Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal structures. Integrative and comparative biology, 47(2).
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  Evolutionary diversifications are commonly attributed to the continued modifications of a conserved genetic toolkit of developmental pathways, such that complexity and convergence in organismal forms are assumed to be due to similarity in genetic mechanisms or environmental conditions. This approach, however, confounds the causes of organismal development with the causes of organismal differences and, as such, has only limited utility for addressing the cause of evolutionary change. Molecular mechanisms that are closely involved in both developmental response to environmental signals and major evolutionary innovations and diversifications are uniquely suited to bridge this gap by connecting explicitly the causes of within-generation variation with the causes of divergence of taxa. Developmental pathways of bone formation and a common role for bone morphogenetic proteins (BMPs) in both epigenetic bone remodeling and the evolution of major adaptive diversifications provide such opportunity. We show that variation in timing of ossification can result in similar phenotypic patterns through epigenetically induced changes in gene expression and propose that both genetic accommodation of environmentally induced developmental pathways and flexibility in development across environments evolve through heterochronic shifts in bone maturation relative to exposure to unpredictable environments. We suggest that such heterochronic shifts in ossification can not only buffer development under fluctuating environments while maintaining epigenetic sensitivity critical for normal skeletal formation, but also enable epigenetically induced gene expression to generate specialized morphological adaptations. We review studies of environmental sensitivity of BMP pathways and their regulation of formation, remodeling, and repair of cartilage and bone to examine the hypothesis that BMP-mediated skeletal adaptations are facilitated by evolved reactivity of BMPs to external signals. Surprisingly, no empirical study to date has identified the molecular mechanism behind developmental plasticity in skeletal traits. We outline a conceptual framework for future studies that focus on mediation of phenotypic plasticity in skeletal development by the patterns of BMP expression.
• Badyaev, A., Young, R. L., Haselkorn, T. S., & Badyaev, A. -. (2007). Functional equivalence of morphologies enables morphological and ecological diversity. Evolution; international journal of organic evolution, 61(11).
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  Diversity in organismal forms among taxa is thought to reflect distinct selection pressures across environments. The central assumption underlying this expectation is that taxa experiencing similar selection have similar response to that selection. However, because selection acts on trait function, taxa similarity in selection response depends crucially on the relationship between function and morphology. Further, when a trait consists of multiple parts, changes in function in response to selection can result from modification of different parts, and adaptation to the same environment might result in functional but not morphological similarity. Here, we address the extent to which functional and morphological diversity in masticatory apparatus of soricid shrews reflects a shared ecological characteristic of their diet type. We examine the factors limiting morphological variation across shrew species by assessing the relative contribution of trait function (biomechanics of the jaw), ecology, and phylogeny to species similarity in mandibular traits. We found that species that shared diet type were functionally but not morphologically similar. The presence of multiple semi-independently varying traits enabled functional equivalence of composite foraging morphologies and resulted in variable response to selection exerted by similar diet. We show that functional equivalence of multiple morphologies enabled persistence of differences in habitat use (e.g., habitat moisture and coverage) among species that specialize on the same diet. We discuss the importance of developmental and functional integration among traits for evolutionary diversification of morphological structures that generate equivalent functions.
• Duckworth, R. A., & Badyaev, A. V. (2007). Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proceedings of the National Academy of Sciences of the United States of America, 104(38), 15017-15022.
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  PMID: 17827278;PMCID: PMC1986605;Abstract: Behaviors can facilitate colonization of a novel environment, but the mechanisms underlying this process are poorly understood. On one hand, behavioral flexibility allows for an immediate response of colonizers to novel environments, which is critical to population establishment and persistence. On the other hand, integrated sets of behaviors that display limited flexibility can enhance invasion success by coupling behaviors with dispersal strategies that are especially important during natural range expansions. Direct observations of colonization events are required to determine the mechanisms underlying changes in behavior associated with colonization, but such observations are rare. Here, we studied changes in aggression on a large temporal and spatial scale across populations of two sister taxa of bluebirds (Sialia) to show that coupling of aggression and dispersal strongly facilitated the range expansion of western bluebirds across the northwestern United States over the last 30 years. We show that biased dispersal of highly aggressive males to the invasion front allowed western bluebirds to displace less aggressive mountain bluebirds. However, once mountain bluebirds were excluded, aggression of western bluebirds decreased rapidly across consecutive generations in concordance with local selection on highly heritable aggressive behavior. Further, the observed adaptive microevolution of aggression was accelerated by the link between dispersal propensity and aggression. Importantly, our results show that behavioral changes among populations were not caused by behavioral flexibility and instead strongly implicate adaptive integration of dispersal and aggression in facilitating the ongoing and rapid reciprocal range change of these species in North America. © 2007 by The National Academy of Sciences of the USA.
• Jonart, L. M., Hill, G. E., & Badyaev, A. V. (2007). Fighting ability and motivation: determinants of dominance and contest strategies in females of a passerine bird. Animal Behaviour, 74(6), 1675-1681.
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  Abstract: The communication of aggressive motivation or fighting ability has important fitness consequences for competing animals. Selection should favour rapid and honest communication between opponents to settle dominance relationships while avoiding prolonged and intense fighting. We investigated factors that influence fighting strategies and contest outcomes in female house finches, Carpodacus mexicanus, specifically focusing on the following questions. (1) What social contexts trigger an aggressive response? (2) Does body size and condition contribute to female fighting ability? (3) Do contextual factors, such as mate presence, nest status, nest proximity, and site experience contribute to fighting motivation? (4) Does contest intensity and duration increase as the differences in fighting ability between opponents decrease? (5) What is the relative contribution of fighting ability and aggressive motivation to the outcome of a contest? We found that aggression was triggered most frequently by female intrusions in the vicinity of nest and by extrapair female intrusions on an established pair. Female fighting and contest outcomes were strongly influenced by body condition and body size, and females were more motivated to initiate fights and won more contests when their mates were present. Females at the later breeding stages and those fighting closer to their nests were dominant and won more fights compared to females at earlier breeding stages or further from their nests. Females initiated a greater proportion of contests against opponents with similar local familiarity and breeding history. Escalated and prolonged contests, while rare, occurred exclusively between females of the most similar body size and condition. When differences in body condition between opponents are not easily perceived, contestants might escalate contests for more reliable assessments of relative fighting ability. Finally, body condition was not a strong determinant of contest outcome in the contexts with easily assessed differences in the resource value (e.g. mate presence), but without these motivational differences, body condition was the ultimate determinant of contest outcomes. © 2007 The Association for the Study of Animal Behaviour.
• Lindstedt, E. R., Oh, K. P., & Badyaev, A. V. (2007). Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird. Journal of Avian Biology, 38(2), 214-223.
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  Abstract: Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors. © Journal of Avian Biology.
• Young, R. L., & Badyaev, A. V. (2007). Evolution of ontogeny: Linking epigenetic remodeling and genetic adaptation in skeletal structures. Integrative and Comparative Biology, 47(2), 234-244.
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  PMID: 21672834;Abstract: Evolutionary diversifications are commonly attributed to the continued modifications of a conserved genetic toolkit of developmental pathways, such that complexity and convergence in organismal forms are assumed to be due to similarity in genetic mechanisms or environmental conditions. This approach, however, confounds the causes of organismal development with the causes of organismal differences and, as such, has only limited utility for addressing the cause of evolutionary change. Molecular mechanisms that are closely involved in both developmental response to environmental signals and major evolutionary innovations and diversifications are uniquely suited to bridge this gap by connecting explicitly the causes of within-generation variation with the causes of divergence of taxa. Developmental pathways of bone formation and a common role for bone morphogenetic proteins (BMPs) in both epigenetic bone remodeling and the evolution of major adaptive diversifications provide such opportunity. We show that variation in timing of ossification can result in similar phenotypic patterns through epigenetically induced changes in gene expression and propose that both genetic accommodation of environmentally induced developmental pathways and flexibility in development across environments evolve through heterochronic shifts in bone maturation relative to exposure to unpredictable environments. We suggest that such heterochronic shifts in ossification can not only buffer development under fluctuating environments while maintaining epigenetic sensitivity critical for normal skeletal formation, but also enable epigenetically induced gene expression to generate specialized morphological adaptations. We review studies of environmental sensitivity of BMP pathways and their regulation of formation, remodeling, and repair of cartilage and bone to examine the hypothesis that BMP-mediated skeletal adaptations are facilitated by evolved reactivity of BMPs to external signals. Surprisingly, no empirical study to date has identified the molecular mechanism behind developmental plasticity in skeletal traits. We outline a conceptual framework for future studies that focus on mediation of phenotypic plasticity in skeletal development by the patterns of BMP expression.
• Young, R. L., Haselkorn, T. S., & Badyaev, A. V. (2007). Functional equivalence of morphologies enables morphological and ecological diversity. Evolution, 61(11), 2480-2492.
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  PMID: 17725641;Abstract: Diversity in organismal forms among taxa is thought to reflect distinct selection pressures across environments. The central assumption underlying this expectation is that taxa experiencing similar selection have similar response to that selection. However, because selection acts on trait function, taxa similarity in selection response depends crucially on the relationship between function and morphology. Further, when a trait consists of multiple parts, changes in function in response to selection can result from modification of different parts, and adaptation to the same environment might result in functional but not morphological similarity. Here, we address the extent to which functional and morphological diversity in masticatory apparatus of soricid shrews reflects a shared ecological characteristic of their diet type. We examine the factors limiting morphological variation across shrew species by assessing the relative contribution of trait function (biomechanics of the jaw), ecology, and phylogeny to species similarity in mandibular traits. We found that species that shared diet type were functionally but not morphologically similar. The presence of multiple semi-independently varying traits enabled functional equivalence of composite foraging morphologies and resulted in variable response to selection exerted by similar diet. We show that functional equivalence of multiple morphologies enabled persistence of differences in habitat use (e.g., habitat moisture and coverage) among species that specialize on the same diet. We discuss the importance of developmental and functional integration among traits for evolutionary diversification of morphological structures that generate equivalent functions. © 2007 The Author(s).
• Badyaev, A. V., Hamstra, T. L., Oh, K. P., & A., D. (2006). Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proceedings of the National Academy of Sciences of the United States of America, 103(39), 14406-14411.
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  PMID: 16983088;PMCID: PMC1599976;Abstract: Duration of developmental stages in animals evolves under contrasting selection pressures of age-specific mortality and growth requirements. When relative importance of these effects varies across environments, evolution of developmental periods is expected to be slow. In birds, maternal effects on egg-laying order and offspring growth, two proximate determinants of nestling period, should enable rapid adjustment of developmental periods to even widely fluctuating mortality rates. We test this hypothesis in a population of house finches (Carpodacus mexicanus) breeding under two contrasting mortality risks: (i) a nest mite-free condition when selection on offspring survival favors a longer time in the nest; and (ii) a mite infestation when selection favors a shorter nest tenure. Mites affected survival of sons more than daughters, and females breeding under mite infestation laid male eggs last and female eggs first in the clutch, thereby reducing sons' exposure to mites and associated mortality. Strong sex bias in laying order and growth patterns enabled mite-infested offspring to achieve similar fledging size, despite a shorter nest tenure, compared with mite-free conditions. In mite-infested nests, male nestlings hatched at larger sizes, completed growth earlier, and had faster initial growth compared with mite-free nests, whereas mite-infested females grew more slowly but for a longer period of time. A combination of heavily sex-biased laying order and sex differences in growth patterns lowered mite-induced mortality by >10% in both sexes. Thus, strong maternal effects can account for frequently observed, but theoretically unexpected, concordance of mortality risks and growth patterns, especially under fluctuating ecological conditions. © 2006 by The National Academy of Sciences of the USA.
• Badyaev, A. V., Oh, K. P., & Mui, R. (2006). Evolution of sex-biased maternal effects in birds: II. Contrasting sex-specific oocyte clustering in native and recently established populations. Journal of Evolutionary Biology, 19(3), 909-921.
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  PMID: 16674587;Abstract: In species that produce broods of multiple offspring, parents need to partition resources among simultaneously growing neonates that often differ in growth requirements. In birds, multiple ovarian follicles develop inside the female at the same time, resulting in a trade-off of resources among them and potentially limiting maternal ability for sex-specific allocation. We compared resource acquisition among oocytes in relation to their future sex and ovulation order in two populations of house finches with contrasting sex-biased maternal strategies. In a native Arizona population, where mothers do not bias offspring sex in relation to ovulation order, the male and female oocytes did not show sex-specific trade-offs of resources during growth and there was no evidence for spatial or temporal segregation of male and female oocytes in the ovary. In contrast, in a recently established Montana population where mothers strongly bias offspring sex in relation to ovulation order, we found evidence for both intra-sexual trade-offs among male and female oocytes and sex-specific clustering of oocytes in the ovary. We discuss the importance of sex-specific resource competition among offspring for the evolution of sex-ratio adjustment and sex-specific maternal resource allocation. © 2005 European Society for Evolutionary Biology.
• Badyaev, A. V., Seaman, D. A., Navara, K. J., Hill, G. E., & Mendonça, M. (2006). Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. Journal of Evolutionary Biology, 19(4), 1044-1057.
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  PMID: 16780506;Abstract: Overlap in growth of offspring should constrain the opportunity for sex-biased maternal effects, yet sex-specific allocation of maternal resources among simultaneously growing ova is often observed in vertebrates. In birds, such allocation can be accomplished either by temporal clustering of ova that become the same sex, resulting in sex-biased egg-laying order, or by follicle-specific delivery of maternal resources. Two house finch populations at the northern and southern boundaries of the species range have opposite ovulation sequences of male and female eggs, and thus, in the absence of sex differences in ova growth or sex-specific maternal strategies, would be expected to have opposite sex-specific accumulation of maternal products. We found that the populations had strong and similar gradients of steroid distribution in relation to ovulation order, whereas distribution of carotenoids and vitamins correlated with each follicle's accumulation of steroids. In both populations, temporal bias in production of sons and daughters within a clutch enabled strongly sex-specific acquisition of maternal products, and oocytes of the same sex were highly interdependent in their accumulation of steroids. Moreover, in nests where the sex-bias in relation to ovulation order deviated from population-specific patterns, eggs had highly distinct concentrations of steroids, carotenoids and vitamins. These results and previous findings of sex-specific yolk partitioning among oocytes suggest that oocytes that become males and females are temporally or spatially clustered during their ovarian growth. We discuss the implication of these findings for the evolution of sex-specific maternal resource allocation. © 2006 The Authors.
• Badyaev, A., Oh, K. P., & Badyaev, A. -. (2006). Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. Proceedings. Biological sciences / The Royal Society, 273(1596).
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  Choice of genetically unrelated mates is widely documented, yet it is not known how self-referential mate choice can co-occur with commonly observed directional selection on sexual displays. Across 10 breeding seasons in a wild bird population, we found strong fitness benefits of matings between genetically unrelated partners and show that self-referential choice of genetically unrelated mates alternates with sexual selection on elaborate plumage. Seasonal cycles of diminishing variation in ornamentation, caused by early pairing of the most elaborated males, and influx of increasingly genetically unrelated available mates caused by female-biased dispersal, lead to temporal fluctuations in the target of mate choice and enabled coexistence of directional selection for ornament elaboration with adaptive pairing of genetically unrelated partners.
• Badyaev, A., Young, R. L., & Badyaev, A. -. (2006). Evolutionary persistence of phenotypic integration: influence of developmental and functional relationships on complex trait evolution. Evolution; international journal of organic evolution, 60(6).
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  Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.
• Dhondt, A. A., Badyaev, A. V., Dobson, A. P., Hawley, D. M., Driscoll, M. J., Hochachka, W. M., & Ley, D. H. (2006). Dynamics of mycoplasmal conjunctivitis in the native and introduced range of the host. EcoHealth, 3(2), 95-102.
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  Abstract: In 1994, Mycoplasma gallisepticum, a common bacterial poultry pathogen, caused an epidemic in house finches in the eastern part of their North American range where the species had been introduced in the 1940s. Birds with mycoplasmal conjunctivitis were reported across the entire eastern United States within 3-4 years. Here we track the course of the Mycoplasma gallisepticum epidemic as it reached native, western North American populations of the house finch. In 2002, Mycoplasma gallisepticum was first observed in a native house finch population in Missoula, MT, where it gradually increased in prevalence during the next 2 years. Concurrently, house finches with conjunctivitis were reported with increasing number in the Pacific Northwest. In native populations of the host, the epidemic expanded more slowly, and reached lower levels of prevalence than in the eastern, introduced range of the species. Maximal prevalence was about half in the Missoula population than in local populations in the East. Although many factors can contribute to these differences, we argue that it is most likely the higher genetic heterogeneity in western than in eastern populations caused the lower impact of the pathogen. © 2006 EcoHealth Journal Consortium.
• Mennill, D. J., Badyaev, A. V., Jonart, L. M., & Hill, G. E. (2006). Male house finches with elaborate songs have higher reproductive performance. Ethology, 112(2), 174-180.
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  Abstract: The elaborate songs of male animals are thought to function in either territory defense (male-male communication) or mate attraction (male-female communication). In non-territorial animals, male vocalizations are expected to function primarily in mate attraction, yet the reproductive consequences of male vocalizations in non-territorial animals are poorly described. Here we explore the relationship between male song and male reproductive performance in a free-living population of house finches, Carpodacus mexicanus, a non-migratory, non-territorial songbird. Based on recordings of 20 males, we analyzed three song features (song length, number of unique syllables per song, and song rate) and compared male song with two measures of within-pair reproductive performance (nest initiation date and clutch size) and one measure of extra-pair reproductive performance (whether males sired extra-pair young). We demonstrate a positive association between male song and within-pair reproductive performance; males that sang long songs initiated their first clutch significantly earlier and males that sang songs at a faster rate had larger clutches. Despite the fact that only one of our recorded males sired extra-pair young in the nest of another male, this male's songs were the most elaborate for two of three song features measured, anecdotally suggesting that male song may play a role in both within-pair and extra-pair partner choice. These results suggest that male song is a sexually selected trait in non-territorial house finches. © 2006 Blackwell Verlag.
• Navara, K. J., Badyaev, A. V., Mendonça, M. T., & Hill, G. E. (2006). Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiological and Biochemical Zoology, 79(6), 1098-1105.
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  PMID: 17041875;Abstract: The manipulation of egg content is one of the few ways by which female birds can alter offspring quality before hatch. Lipid-soluble vitamins and carotenoids are potent antioxidants. Female birds deposit these antioxidants into eggs in variable amounts according to environmental and social conditions, and the quantities deposited into eggs can have effects on offspring health and immunological condition. Allocation theory posits that females will alter the distribution of resources according to mate quality, sometimes allocating resources according to the differential allocation hypothesis (DAH), investing more in offspring sired by better-quality males, and other times allocating resources according to a compensatory strategy, enhancing the quality of offspring sired by lower-quality males. It is unknown, however, whether antioxidants are deposited into eggs according to the DAH or a compensatory strategy. We examined deposition patterns of yolk antioxidants (including vitamin E and three carotenoids) in relation to laying order, mate attractiveness, female condition, and yolk androgen content in the house finch (Carpodacus mexicanus). Female house finches deposited significantly more total antioxidants into eggs sired by less attractive males. Additionally, yolk antioxidant content was significantly positively correlated with female condition, which suggests a cost associated with the deposition of antioxidants into eggs. Finally, concentrations of antioxidants in egg yolks were positively correlated with total yolk androgen content. We suggest that yolk antioxidants are deposited according to a compensatory deposition strategy, enabling females to improve the quality of young produced with less attractive males. Additionally, yolk antioxidants may act to counter some of the detrimental effects associated with high levels of yolk androgens in eggs and, thus, may exert a complementary effect to yolk androgens. © 2006 by The University of Chicago. All rights reserved.
• Oh, K. P., & Badyaev, A. V. (2006). Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. Proceedings of the Royal Society B: Biological Sciences, 273(1596), 1913-1919.
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  Abstract: Choice of genetically unrelated mates is widely documented, yet it is not known how self-referential mate choice can co-occur with commonly observed directional selection on sexual displays. Across 10 breeding seasons in a wild bird population, we found strong fitness benefits of matings between genetically unrelated partners and show that self-referential choice of genetically unrelated mates alternates with sexual selection on elaborate plumage. Seasonal cycles of diminishing variation in ornamentation, caused by early pairing of the most elaborated males, and influx of increasingly genetically unrelated available mates caused by female-biased dispersal, lead to temporal fluctuations in the target of mate choice and enabled coexistence of directional selection for ornament elaboration with adaptive pairing of genetically unrelated partners. © 2006 The Royal Society.
• Oh, K. P., & Badyaev, A. V. (2006). Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits.. Proceedings. Biological sciences / The Royal Society, 273(1596), 1913-1919.
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  PMID: 16822752;PMCID: PMC1634773;Abstract: Choice of genetically unrelated mates is widely documented, yet it is not known how self-referential mate choice can co-occur with commonly observed directional selection on sexual displays. Across 10 breeding seasons in a wild bird population, we found strong fitness benefits of matings between genetically unrelated partners and show that self-referential choice of genetically unrelated mates alternates with sexual selection on elaborate plumage. Seasonal cycles of diminishing variation in ornamentation, caused by early pairing of the most elaborated males, and influx of increasingly genetically unrelated available mates caused by female-biased dispersal, lead to temporal fluctuations in the target of mate choice and enabled coexistence of directional selection for ornament elaboration with adaptive pairing of genetically unrelated partners.
• Young, R. L., & Badyaev, A. V. (2006). Evolutionary persistence of phenotypic integration: Influence of developmental and functional relationships on complex trait evolution. Evolution, 60(6), 1291-1299.
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  PMID: 16892978;Abstract: Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species. © 2006 The Society for the Study of Evolution. All rights reserved.
• Badyaev, A. V. (2005). Maternal inheritance and rapid evolution of sexual size dimorphism: Passive effects or active strategies?. American Naturalist, 166(4 SUPPL.), S17-S30.
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  PMID: 16224709;Abstract: Adaptive evolution is often strongly influenced by maternal inheritance that transfers the parental strategies across generations. The consequences of maternal effects for the offspring generation depend on the between-generation similarity in environments and on the evolved sensitivity of the offspring's ontogeny to maternal effects. When these factors differ between sons and daughters, maternal effects can influence the evolution of sexual dimorphism. The establishment of house finch populations across western Montana during the last 30 years was accompanied by rapid evolutionary change in sexual size dimorphism. Here I show that traits that changed the most across generations were most influenced by maternal effects in males but not females. Maternal effects differentially affected sons' and daughters' survival; greater maternal effects were commonly associated with higher survival of sons, especially when maternal and offspring environments were similar. Stronger maternal effects extended preselection phenotypic variance in morphological traits of males, thereby producing some locally adaptive phenotypes and lessening juvenile mortality. Thus, the observed sex-specific maternal effects and their contribution to the evolution of sexual size dimorphism are likely a passive consequence of the distinct sensitivity of sons and daughters to maternal adaptations to breeding in ecologically distinct parts of the house finch's expanding range. © 2005 by The University of Chicago.
• Badyaev, A. V. (2005). Role of stress in evolution: From individual adaptability to evolutionary adaptation. Variation, 277-302.
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  Abstract: Lack of a developmental perspective in evolutionary studies of stress has left researchers with several unresolved questions. First, how can organisms prepare for novel and extreme environmental change? The organismal ability to mount an appropriate reaction to a stressor requires recognition and evaluation of the extreme environment. How can this ability evolve in relation to stressors that are short and rare in relation to a species generation time? Stress occurs when changes in the external or internal environment are interpreted by an organism as a threat to its homeostasis. The ability of an organism to mount an appropriate response to potentially stressful environmental changes requires correct recognition of environmental change and the activation of a stress response. The costs and benefits of stress detection and stress response implementation and the costs and benefits of maintaining stress resistance strategies vary among environments and individuals, favoring multiple solutions of dealing with stress. Numerous studies have documented an increase in phenotypic and genotypic variance under stress, and it is suggested that this variance is a source of novel adaptations under changed environments. The Chapter outlines this perspective, with specific focus on the effect of stress during development in animals and suggests that these questions are resolved by considering the organization of developmental systems that enable accommodation and channeling of stress-induced variation without compromising organismal functionality; the significance of phenotypic and genetic assimilation of neurological, physiological, morphological, and behavioral responses to stressors; as well as multiple inheritance systems that transfer the wide array or developmental resources and conditions between the generations enabling long-term persistence and evolution of stress-induced adaptations. © 2005 Elsevier Inc. All rights reserved.
• Badyaev, A. V. (2005). Stress-induced variation in evolution: From behavioural plasticity to genetic assimilation. Proceedings of the Royal Society B: Biological Sciences, 272(1566), 877-886.
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  PMID: 16024341;PMCID: PMC1564094;Abstract: Extreme environments are closely associated with phenotypic evolution, yet the mechanisms behind this relationship are poorly understood. Several themes and approaches in recent studies significantly further our understanding of the importance that stress-induced variation plays in evolution. First, stressful environments modify (and often reduce) the integration of neuroendocrinological, morphological and behavioural regulatory systems. Second, such reduced integration and subsequent accommodation of stress-induced variation by developmental systems enables organismal 'memory' of a stressful event as well as phenotypic and genetic assimilation of the response to a stressor. Third, in complex functional systems, a stress-induced increase in phenotypic and genetic variance is often directional, channelled by existing ontogenetic pathways. This accounts for similarity among individuals in stress-induced changes and thus significantly facilitates the rate of adaptive evolution. Fourth, accumulation of phenotypically neutral genetic variation might be a common property of locally adapted and complex organismal systems, and extreme environments facilitate the phenotypic expression of this variance. Finally, stress-induced effects and stress-resistance strategies often persist for several generations through maternal, ecological and cultural inheritance. These transgenerational effects, along with both the complexity of developmental systems and stressor recurrence, might facilitate genetic assimilation of stress-induced effects. Accumulation of phenotypically neutral genetic variance by developmental systems and phenotypic accommodation of stress-induced effects, together with the inheritance of stress-induced modifications, ensure the evolutionary persistence of stress-response strategies and provide a link between individual adaptability and evolutionary adaptation. © 2005 The Royal Society.
• Badyaev, A. V., Foresman, K. R., & Young, R. L. (2005). Evolution of morphological integration: Developmental accommodation of stress-induced variation. American Naturalist, 166(3), 382-395.
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  PMID: 16224692;Abstract: Extreme environmental change during growth often results in an increase in developmental abnormalities in the morphology of an organism. The evolutionary significance of such stress-induced variation depends on the recurrence of a stressor and on the degree to which developmental errors can be accommodated by an organism's ontogeny without significant loss of function. We subjected populations of four species of soricid shrews to an extreme environment during growth and measured changes in the patterns of integration and accommodation of stress-induced developmental errors in a complex of mandibular traits. Adults that grew under an extreme environment had lower integration of morphological variation among mandibular traits and highly elevated fluctuating asymmetry in these traits, compared to individuals that grew under the control conditions. However, traits differed strongly in the magnitude of response to a stressor - traits within attachments of the same muscle (functionally integrated traits) had lower response and changed their integration less than other traits. Cohesiveness in functionally integrated complexes of traits under stress was maintained by close covariation of their developmental variation. Such developmental accommodation of stress-induced variation might enable the individual's functioning and persistence under extreme environmental conditions and thus provides a link between individual adaptation to stress and the evolution of stress resistance. © 2005 by The University of Chicago.
• Badyaev, A. V., Schwabl, H., Young, R. L., Duckworth, R. A., Navara, K. J., & Parlow, A. F. (2005). Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proceedings of the Royal Society B: Biological Sciences, 272(1577), 2165-2172.
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  PMID: 16188605;PMCID: PMC1559945;Abstract: Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range. © 2005 The Royal Society.
• Badyaev, A., & Badyaev, A. -. (2005). Maternal inheritance and rapid evolution of sexual size dimorphism: passive effects or active strategies?. The American naturalist, 166 Suppl 4.
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  Adaptive evolution is often strongly influenced by maternal inheritance that transfers the parental strategies across generations. The consequences of maternal effects for the offspring generation depend on the between-generation similarity in environments and on the evolved sensitivity of the offspring's ontogeny to maternal effects. When these factors differ between sons and daughters, maternal effects can influence the evolution of sexual dimorphism. The establishment of house finch populations across western Montana during the last 30 years was accompanied by rapid evolutionary change in sexual size dimorphism. Here I show that traits that changed the most across generations were most influenced by maternal effects in males but not females. Maternal effects differentially affected sons' and daughters' survival; greater maternal effects were commonly associated with higher survival of sons, especially when maternal and offspring environments were similar. Stronger maternal effects extended preselection phenotypic variance in morphological traits of males, thereby producing some locally adaptive phenotypes and lessening juvenile mortality. Thus, the observed sex-specific maternal effects and their contribution to the evolution of sexual size dimorphism are likely a passive consequence of the distinct sensitivity of sons and daughters to maternal adaptations to breeding in ecologically distinct parts of the house finch's expanding range.
• Badyaev, A., & Badyaev, A. -. (2005). Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proceedings. Biological sciences / The Royal Society, 272(1566).
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  Extreme environments are closely associated with phenotypic evolution, yet the mechanisms behind this relationship are poorly understood. Several themes and approaches in recent studies significantly further our understanding of the importance that stress-induced variation plays in evolution. First, stressful environments modify (and often reduce) the integration of neuroendocrinological, morphological and behavioural regulatory systems. Second, such reduced integration and subsequent accommodation of stress-induced variation by developmental systems enables organismal 'memory' of a stressful event as well as phenotypic and genetic assimilation of the response to a stressor. Third, in complex functional systems, a stress-induced increase in phenotypic and genetic variance is often directional, channelled by existing ontogenetic pathways. This accounts for similarity among individuals in stress-induced changes and thus significantly facilitates the rate of adaptive evolution. Fourth, accumulation of phenotypically neutral genetic variation might be a common property of locally adapted and complex organismal systems, and extreme environments facilitate the phenotypic expression of this variance. Finally, stress-induced effects and stress-resistance strategies often persist for several generations through maternal, ecological and cultural inheritance. These transgenerational effects, along with both the complexity of developmental systems and stressor recurrence, might facilitate genetic assimilation of stress-induced effects. Accumulation of phenotypically neutral genetic variance by developmental systems and phenotypic accommodation of stress-induced effects, together with the inheritance of stress-induced modifications, ensure the evolutionary persistence of stress-response strategies and provide a link between individual adaptability and evolutionary adaptation.
• Badyaev, A. V. (2004). Developmental perspective on the evolution of sexual ornaments. Evolutionary Ecology Research, 6(7), 975-991.
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  Abstract: Sexual ornaments are favoured to be both less integrated with other organismal traits for greater expression, and yet more integrated with organismal development and functions to better indicate the physiological quality of an organism. Two conceptual approaches in morphological evolution - the consideration of internal and external processes and the evolution of integration and modularity - are useful in resolving this apparent paradox, yet these approaches are mostly overlooked in studies of the development of sexual displays. Moreover, whereas recent studies have recognized the evolutionary continuum of the mechanisms by which sexual selection operates, the consequences for the evolution of development of sexual displays are not well understood. Here I suggest that the concept of morphological integration may provide a useful framework for understanding the development and evolution of sexual ornamentation.
• Badyaev, A. V., & Foresman, K. R. (2004). Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. American Naturalist, 163(6), 868-879.
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  PMID: 15266384;Abstract: Stress-induced deviations from normal development are often assumed to be random, yet their accumulation and expression can be influenced by patterns of morphological integration within an organism. We studied within-individual developmental variation (fluctuating asymmetry) in the mandible of four shrew species raised under normal and extreme environments. Patterns of among-individual variation and fluctuating asymmetry were strongly concordant in traits that were involved in the attachment of the same muscles (i.e., functionally integrated traits), and fluctuating asymmetry was closely integrated among these traits, implying direct developmental interactions among traits involved in the same function. Stress-induced variation was largely confined to the directions delimited by functionally integrated groups of traits in the pattern that was concordant with species divergence - species differed most in the same traits that were most sensitive to stress within each species. These results reveal a strong effect of functional complexes on directing and incorporating stress-induced variation during development and might explain the historical persistence of sets of traits involved in the same function in shrew jaws despite their high sensitivity to environmental variation.
• Badyaev, A. V., & Young, R. L. (2004). Complexity and integration in sexual ornamentation: An example with carotenoid and melanin plumage pigmentation. Journal of Evolutionary Biology, 17(6), 1317-1327.
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  PMID: 15525416;Abstract: Sexual ornaments often consist of several components produced by distinct developmental processes. The complexity of sexual ornaments might be favoured by mate choice of individual components in different environments which ultimately results in weak interrelationships (integration) among the developmental processes that produce these components. At the same time, sexual selection for greater exaggeration of individual components favours their stronger co-dependence on organismal resources. This should ultimately produce stronger condition-mediated integration among ornaments' components in individuals with the most exaggerated ornamentation. Here we distinguish between these two sources of integration by examining the relationship between integration and elaboration of sexual ornamentation in three bird species: two with carotenoid-based sexual ornamentation (the house finch, Carpodacus mexicanus and common redpoll, Carduelis flammea) and a species with melanin-based sexual ornamentation (house sparrow, Passer domesticus). We found that integration of components varied with elaboration of carotenoid-based ornamentation but not of melanin ornamentation. In the house finches, integration was the highest in individuals with small ornaments and decreased with ornament elaboration whereas the pattern was the opposite in common redpolls. These results suggest that in these species integration and complexity of carotenoid-based ornamental components are due to shared condition-dependence of distinct developmental pathways, whereas integration and complexity of the melanin ornamentation is due to organismal integration of developmental pathways and is largely condition-and environment-invariant. Thus, functionally, ornamentation of the house sparrows can be considered a single trait, whereas complexity of the house finch and redpoll ornamentation varies with ornament elaboration and individual condition.
• Sæther, B., Engen, S., Møller, A. P., Weimerskirch, H., Visser, M. E., Fiedler, W., Matthysen, E., Lambrechts, M. M., Badyaev, A., Becker, P. H., Brommer, J. E., Bukacinski, D., Bukacinska, M., Christensen, H., Dickinson, J., Feu, C. D., Gehlbach, F. R., Heg, D., Hötker, H., , Merilä, J., et al. (2004). Life-history variation predicts the effects of demographic stochasticity on avian population dynamics. American Naturalist, 164(6), 793-802.
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  Abstract: Comparative analyses of avian population fluctuations have shown large interspecific differences in population variability that have been difficult to relate to variation in general ecological characteristics. Here we show that interspecific variation in demographic stochasticity, caused by random variation among individuals in their fitness contributions, can be predicted from a knowledge of the species' position along a "slow-fast" gradient of life-history variation, ranging from high reproductive species with short life expectancy at one end to species that often produce a single offspring but survive well at the other end of the continuum. The demographic stochasticity decreased with adult survival rate, age at maturity, and generation time or the position of the species toward the slow end of the slow-fast life-history gradient. This relationship between life-history characteristics and demographic stochasticity was related to interspecific differences in the variation among females in recruitment as well as to differences in the individual variation in survival. Because reproductive decisions in birds are often subject to strong natural selection, our results provide strong evidence for adaptive modifications of reproductive investment through life-history evolution of the influence of stochastic variation on avian population dynamics.
• Young, R. L., & Badyaev, A. V. (2004). Evolution of sex-biased maternal effects in birds: I. Sex-specific resource allocation among simultaneously growing oocytes. Journal of Evolutionary Biology, 17(6), 1355-1366.
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  PMID: 15525420;Abstract: Females in species that produce broods of multiple offspring need to partition resources among simultaneously growing ova, embryos or neonates. In birds, the duration of growth of a single egg exceeds the ovulation interval, and when maternal resources are limited, a temporal overlap among several developing follicles in the ovary might result in a trade-off of resources among them. We studied growth of oocytes in relation to their future ovulation order, sex, and overlap with other oocytes in a population of house finches (Carpodacus mexicanus) where strongly sex-biased maternal effects are favoured by natural selection. We found pronounced differences in growth patterns between oocytes that produced males and females. Male oocytes grew up to five times faster and reached their ovulation size earlier than female oocytes. Early onset and early termination of male oocytes' growth in relation to their ovulation resulted in their lesser temporal overlap with other growing ova compared with female oocytes. Consequently, ovulation mass of female but not male oocytes was strongly negatively affected by temporal overlap with other oocytes. In turn, mass of male oocytes was mostly affected by the order of ovulation and by maternal incubation strategy. These results provide a mechanism for sex-biased allocation of maternal resources during egg formation and provide insights into the timing of the sex-determining meiotic division in relation to ovulation in this species.
• Badyaev, A. V., & Duckworth, R. A. (2003). Context-dependent sexual advertisement: Plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird. Journal of Evolutionary Biology, 16(6), 1065-1076.
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  PMID: 14640398;Abstract: Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state- and context-specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition-dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus) - a species that develops a new sexual ornament once a year after breeding. Throughout males' lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season - males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post-juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition-dependence of ornamentation sharply decreased throughout a male's lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context-dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a male's life.
• Badyaev, A. V., & Hill, G. E. (2003). Avian Sexual Dichromatism in Relation to Phylogeny and Ecology. Annual Review of Ecology, Evolution, and Systematics, 34, 27-49.
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  Abstract: The extent and diversity of sexual dichromatism in birds is thought to be due to the intensity of current sexual selection on the plumage ornamentation of males and females. This view leads to an expectation of concordance between ecological conditions and sexual dichromatism. Yet, because expression of dichromatism is the result of not only current selection, but also historical patterns of development, function, and selection, the concordance between ecology and current sexual dichromatism is not straightforward. Recent studies have revealed a number of trends in the evolution of avian sexual ornamentation that seem contrary to what is expected if current sexual selection is the primary force shaping dichromatism. For example, change in sexual dichromatism is often the result of evolutionary changes in female rather than male ornamentation. Moreover, sexual dichromatism is often an ancestral rather than a derived state; current expression of dichromatism is frequently the result of selection for lesser ornamentation in one sex and not for ornament elaboration. Loss and gain of sexual ornamentation sometimes precedes changes in preference for sexual ornamentation, and sexual ornaments can have high evolutionary lability despite their developmental and functional complexity. These findings emphasize that phylogenetic reconstructions must play a central role in attempts to understand the function and evolution of sexual dichromatism. With a historical perspective, one can test the relative importance of direct selection, indirect selection, and drift in relation to changes of sexual dichromatism. If sexual selection is invoked, the mechanisms of sexual selection can be explored by examining the concordance between the elaboration of ornamentation and the preferences for ornamentation across species and by tracing phylogenetic trajectories of sexual ornaments. Finally, placing physiological, genetic, and developmental mechanisms of sexual ornamentation into such a phylogenetic framework will enable greater inference about the past evolution and current function of sexual dichromatism in birds.
• Badyaev, A. V., Beck, M. C., Hill, G. E., & Whittingham, L. A. (2003). The evolution of sexual size dimorphism in the house finch. V. Maternal effects. Evolution, 57(2), 384-396.
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  PMID: 12683534;Abstract: The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.
• Badyaev, A. V., Hill, G. E., & Beck, M. L. (2003). Interaction between maternal effects: Onset of incubation and offspring sex in two populations of a passerine bird. Oecologia, 135(3), 386-390.
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  PMID: 12721828;Abstract: Maternal phenotype and maternal environment can profoundly affect the phenotype and fitness of offspring. Yet the causes of variation in such maternal effects are rarely known. Embryos in avian eggs cannot develop without being incubated and this creates an opportunity for maternal control of duration and onset of offspring development. However, females might adjust the start of incubation (e.g., coincident with the first egg or delayed until after egg-laying) in response to environmental conditions that they experience at the time of breeding. We studied two populations of the house finch (Carpodacus mexicanus) that breed at the climatic extremes of the species' geographical range (Montana and Alabama) and found that in both populations, the timing of incubation onset was closely associated with the bias in the sequence in which male and female eggs were laid within a clutch. When females started incubation with the first egg, they produced sons and daughters in highly biased sequence, when females delayed the onset of incubation until after the egg-laying, the sequence of sons and daughters was not biased. Because in both populations, onset of incubation was associated with the ambient temperature, these results emphasize that maternal effects on offspring can be influenced by ecological conditions experienced by parental generation.
• Ballentine, B., Badyaev, A., & Hill, G. E. (2003). Changes in song complexity correspond to periods of female fertility in blue grosbeaks (Guiraca caerulea). Ethology, 109(1), 55-66.
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  Abstract: Song complexity is thought to be a sexually selected trait in passerine birds; however, quantifying relevant parameters of song complexity is the first step in testing the theory that song complexity is a sexually selected trait. We show here that blue grosbeak (Guiraca caerulea) males sing a single song type but the properties of that song type vary between renditions. This pattern of song delivery potentially provides females with an opportunity to assess dimensions of song complexity other then repertoire size. Here we characterize song complexity using four measures: (i) element repertoire size, (ii) proportion of distinct song variant, (iii) song versatility, and (iv) syntax consistency. We studied the functional significance of song complexity by comparing measures of song complexity before and after periods of female fertility. We found that male blue grosbeaks sing more song variants, use more versatile arrangements of elements, and maintain more syntax consistency during the fertile period of their social mate than during their social mate's non-fertile period. These results point to a functional relationship between changes in song complexity and periods of female fertility in this species.
• Duckworth, R. A., Badyaev, A. V., & Parlow, A. F. (2003). Elaborately ornamented males avoid costly parental care in the house finch (Carpodacus mexicanus): A proximate perspective. Behavioral Ecology and Sociobiology, 55(2), 176-183.
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  Abstract: Selection should favor flexibility in reproductive tactics when the combination of sexual traits and reproductive behaviors that achieve the highest fitness differs between males within a population. Understanding the functional significance of variation in male reproductive tactics can provide insight into their evolution. Male house finches (Carpodacus mexicanus) in a Montana population display continuous variation in parental tactics: males with more elaborated (redder) plumage color provide little or no parental care compared to less elaborated (dull) males. Here, we first determined whether elevation of prolactin (a pituitary hormone) was related to variation in male parental tactics and, second, we used the relationship between prolactin levels and parental behavior to investigate why redder males avoid a high investment in parental care. We found that prolactin elevation was closely associated with paternal care. In addition, males with redder plumage color had low prolactin levels, whereas dull males, which provision twice as frequently, had high levels of prolactin. We also found that male condition was unrelated to plumage color but negatively related to prolactin levels. These results suggest that the low provisioning of redder males was not due to physiological constraints, but instead reflected a tactic to avoid the costs associated with parental care. The condition benefits accrued by redder males may explain their higher post-breeding survival compared to dull males. Moreover, dull males were previously shown to have higher pairing success than redder males, suggesting that the relationship between male plumage color and parental care may reflect individually optimized parental tactics.
• Duckworth, R. A., Badyaev, A. V., Farmer, K. L., Hill, G. E., & Roberts, S. R. (2003). First case of Mycoplasma gallisepticum infection in the western range of the House Finch (Carpodacus mexicanus). Auk, 120(2), 528-530.
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  Abstract: We report the first case of mycoplasmosis in the western range of the House Finch (Carpodacus mexicanus). This disease originated in the eastern United States and has been previously documented only in eastern introduced House Finch populations where it reached epizootic proportions causing extensive and widespread mortality. Documentation of this disease in western Montana suggests that previously disjunct eastern and western populations of House Finches are now mixing in the northern part of their range. More importantly, as native House Finches are highly susceptible to this novel pathogen, western populations may now be at risk of high mortality, similar to that experienced by non-native eastern populations. Close monitoring of this disease in the western part of the House Finch range will provide important insight into the dynamics of the emerging disease and evolution of resistance to the pathogen.
• Badyaev, A. V. (2002). Growing apart: An ontogenetic perspective on the evolution of sexual size dimorphism. Trends in Ecology and Evolution, 17(8), 369-378.
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  Abstract: Sexes play different roles in reproduction and the adaptive significance of the often remarkably distinct morphologies of adult males and females is documented frequently. Yet, in most vertebrates, the sexes are nearly identical in morphology during early development and undergo highly divergent growth to achieve different adult sizes. The mechanisms that enable the virtually genetically identical sexes to have such divergent growth are not well understood. Of special interest are the constraints that a shared gene pool imposes on sex-specific modifications of growth and the ways that males and females overcome these constraints in response to divergent selection pressures. Recent studies show that the rapid evolution of sex-specific developmental regulators and modifiers can produce sexual dimorphism in size whilst maintaining the integrity of the developmental program that is shared between the sexes.
• Badyaev, A. V., & Hill, G. E. (2002). Avian quick-change artists. Natural History, 111(5), 58-64.
• Badyaev, A. V., & Hill, G. E. (2002). Paternal care as a conditional strategy: Distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch. Behavioral Ecology, 13(5), 591-597.
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  Abstract: When individuals in a population differ in physiological condition and residual reproductive value, selection should favor phenotypic plasticity in reproductive investment such that individuals are able to adopt the reproductive tactic that results in the highest fitness under given conditions. Here we examined reproductive tactics in relation to the elaboration of condition-dependent sexual ornamentation (carotenoid breast coloration) in a Montana population of the house finches (Carpodacus mexicanus). Males used distinct reproductive tactics depending on elaboration of their sexual ornamentation. Males with red pigmentation (maximum ornament elaboration) paired with females that nested earlier, but these males did little provisioning of incubating females and nestlings. In contrast, males with yellow coloration paired with females that nested later, but these males fed female and nestlings more. Consequently, for red males offspring recruitment was primarily affected by earlier nest initiation, whereas in yellow males it was affected most by male provisioning. In males with intermediate plumage coloration, all measured components, nest initiation, provisioning of incubating female, and nestling feeding, strongly contributed to offspring recruitment. The fitness consequences of alternative reproductive tactics of males were influenced by breeding experience and fidelity, of their mates. Among first-time breeders, red males achieved the highest fecundity because of the advantage gained through early nesting and pairing with more experienced females and because of compensation by their mates for low male provisioning of nestlings. Among experienced breeders, males with intermediate plumage coloration achieved the highest fecundity because of the combined benefits of relatively early pairing and high parental care. High variation in sexual ornamentation in a Montana population of house finches may favor distinct associations of sexual displays with a particular set of reproductive behaviors.
• Badyaev, A. V., & Qvarnström, A. (2002). Putting sexual traits into the context of an organism: A life-history perspective in studies of sexual selection. Auk, 119(2), 301-310.
• Badyaev, A. V., Hill, G. E., & Weckworth, B. V. (2002). Species divergence in sexually selected traits: Increase in song elaboration is related to decrease in plumage ornamentation in finches. Evolution, 56(2), 412-419.
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  PMID: 11926507;Abstract: Elaborate plumage and complex songs of male birds are two of the best-known examples of sexually selected traits, yet the interaction between these traits is poorly understood. Theory suggests that among a suite of potential displays, animals will emphasize traits that are most conspicuous, least costly, or best signal condition and reduce display of other traits. Here we examined the relationship between song and plumage elaborations in cardueline finches, songbirds that are highly variable in plumage displays and songs, but that share a similar mating system. We statistically controlled for body mass, habitat characteristics, and phylogenetic relationships and found that across species song complexity was strongly negatively related to elaboration of plumage ornamentation. When plumage coloration was partitioned into carotenoid-based and melanin-based components, song complexity was negatively related to elaboration of male carotenoid-based coloration but unrelated to elaboration of melanin-based coloration. These observations support the idea that, for condition-dependent traits, animal species trade off trait expression in response to changes in the costs or the information content of these traits. We discuss several alternative explanations for the observed pattern.
• Badyaev, A. V., Hill, G. E., & Whittingham, L. A. (2002). Population consequences of maternal effects: Sex-bias in egg-laying order facilitates divergence in sexual dimorphism between bird populations. Journal of Evolutionary Biology, 15(6), 997-1003.
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  Abstract: When costs and benefits of raising sons and daughters differ between environments, parents may be selected to modify their investment into male and female offspring. In two recently colonized environments, breeding female house finches (Carpodacus mexicanus) modified the sex and growth of their offspring in relation to the order in which eggs were laid in a clutch. Here we show that, in both populations, these maternal effects strongly biased frequency distribution of tarsus size of fully grown males and females and ultimately produced population divergence in this trait. Although in each population, male and female offspring show a wide range of growth patterns, maternal modifications of sex-ratio in relation to egg-laying order resulted in under-representation of the morphologies that were selected against and over-representation of morphologies that were favoured by the local selection on juveniles. The result of these maternal adjustments was fast phenotypic change in sexual size dimorphism within and between populations. Maternal manipulations of offspring morphologies may be especially important at the initial stages of population establishment in the novel environments and may have facilitated recent colonization of much of North America by the house finch.
• Badyaev, A. V., Hill, G. E., Beck, M. L., Dervan, A. A., Duckworth, R. A., McGraw, K. J., Nolan, P. M., & Whittingham, L. A. (2002). Sex-biased hatching order and adaptive population divergence in a passerine bird. Science, 295(5553), 316-318.
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  PMID: 11786641;Abstract: Most species of birds can lay only one egg per day until a dutch is complete, and the order in which eggs are laid often has strong and sex-specific effects on offspring growth and survival. In two recently established populations of the house finch (Carpodacus mexicanus) in Montana and Alabama, breeding females simultaneously adjusted the sex and growth of offspring in relation to their position in the laying order, thereby reducing the mortality of sons and daughters by 10 to 20% in both environments. We show experimentally that the reduction in mortality is produced by persistent and sex-specific maternal effects on the growth and morphology of offspring. These strong parental effects may have facilitated the rapid adaptive divergence among populations of house finches.
• Creech, M., & Badyaev, A. V. (2002). Not quite ubiquitous [2] (multiple letters). Natural History, 111(7), 12-.
• Badyaev, A. V., & Ghalambor, C. K. (2001). Evolution of life histories along elevational gradients: Trade-off between parental care and fecundity. Ecology, 82(10), 2948-2960.
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  Abstract: Life history responses to environmental conditions include a combination of fecundity-survival schedules and behavioral strategies that yield the highest fitness in a given environment. In this study, we examined the pattern of covariation in avian life history strategies along an elevational gradient by comparing variation in life history traits, including most components of parental care, between phylogenetically paired taxa from low- and high-elevation sites. We found that high-elevation species had significantly lower annual fecundity but provided greater parental care to their offspring. However, a strong negative relationship between offspring number and duration of parental care along the elevational gradient suggested that high-elevation species were shifting investment from offspring number toward offspring quality. Although adult survival did not differ between high- and low-elevation species, higher juvenile survival may have compensated for lower annual fecundity in high-elevation species. The elevation at which breeding occurred strongly influenced the partitioning of parental behavior between sexes. Male participation in nestling provisioning was significantly greater in high-elevation species. In turn, altitudinal variation in the frequency of biparental care closely covaries with the intensity of sexual selection, ultimately resulting in the strong elevational pattern of sexual dimorphism. Moreover, elevational variation in costs of development and maintenance of secondary sexual traits constitutes an additional effect on fecundity-survival schedules along elevational gradients. Thus, a trade-off between fecundity and parental care, and associated interactions among morphological, life history, and behavioral traits play important roles in the evolution of life history strategies in birds.
• Badyaev, A. V., Hill, G. E., & Whittingham, L. A. (2001). The evolution of sexual size dimorphism in the house finch. Iv. Population divergence in ontogeny. Evolution, 55(12), 2534-2549.
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  PMID: 11831668;Abstract: Differences among taxa in sexual size dimorphism of adults can be produced by changes in distinct developmental processes and thus may reflect different evolutionary histories. Here we examine whether divergence in sexual dimorphism of adults between recently established Montana and Alabama populations of the house finch (Carpodacus mexicanus) can be attributed to population differences in growth of males and females. In both populations, males and females were similar at hatching, but as a result of sex-specific growth attained sexual size dimorphism by the time of independence. Timing and extent of growth varied between the sexes: Females maintained maximum rates of growth for a longer time than males, whereas males had higher initial growth rates and achieved maximum growth earlier and at smaller sizes than females. Ontogeny of sexual dimorphism differed between populations, but in each population, sexual dimorphism in growth parameters and sexual dimorphism at the time of nest leaving were similar to sexual dimorphism of adults. Variation in growth of females contributed more to population divergence than did growth of males. In each population, we found close correspondence between patterns of sexual dimorphism in growth and population divergence in morphology of adults: Traits that were the most sexually dimorphic in growth in each population contributed the most to population divergence in both sexes. We suggest that sex-specific expression of phenotypic and genetic variation throughout the ontogeny of house finches can result in different responses to selection between males and females of the same age, and thus produce fast population divergence in the sexual size dimorphism.
• Badyaev, A. V., Whittingham, L. A., & Hill, G. E. (2001). The evolution of sexual size dimorphism in the house finch. III. Developmental basis. Evolution, 55(1), 176-189.
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  PMID: 11263737;Abstract: Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.
• Klingenberg, C. P., Badyaev, A. V., Sowry, S. M., & Beckwith, N. J. (2001). Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings. American Naturalist, 157(1), 11-23.
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  PMID: 18707232;Abstract: Organisms are built from distinct modules, which are internally coherent but flexible in their relationships among one another. We examined morphological variation within and between two candidate modules: the fore- and hindwings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the techniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principal component analysis revealed patterns of variation that were remarkably similar for individual variation and fluctuating asymmetry (FA). Because covariation of FA among parts must be due to direct transmission of the developmental perturbations causing FA, this agreement of patterns suggests that much of individual variation is also due to direct developmental interactions within each developing wing. Moreover, partial least squares analysis indicated that the patterns of shape covariation between fore- and hindwings were nearly the same as the patterns of within-wing variation. Shape covariation of FA was only found in bees that had been reared under elevated CO2 concentration but not in bees from the control treatment, suggesting that the mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are developmental modules that maintain internal coherence through direct developmental interactions and are connected to each other only by relatively few links that use the system of interactions within modules.
• Badyaev, A. V., & Foresman, K. R. (2000). Extreme environmental change and evolution: Stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proceedings of the Royal Society B: Biological Sciences, 267(1441), 371-377.
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  PMID: 10722219;PMCID: PMC1690536;Abstract: Morphological structures often consist of simpler traits which can be viewed as either integrated (e.g correlated due to functional interdependency) or non-integrated (e.g. functionally independent) traits. The combination of a long-term stabilizing selection on the entire structure with a short-term directional selection on an adaptively important subset of traits should result in long historical persistence of integrated functional complexes, with environmentally induced variation and macroevolutionary change confined mostly to non-integrated traits. We experimentally subjected populations of three closely related species of Sorex shrews to environmental stress. As predicted, we found that most of the variation in shrew mandibular shape was localized between rather than within the functional complexes; the patterns of integration did not change between the species. The stress-induced variation was confined to nonintegrated traits and was highly concordant with the patterns of evolutionary change - species differed in the same set of non-integrated traits which were most sensitive to stress within each species. We suggest that low environmental and genetic canalization of non-integrated traits may have caused these traits to be most sensitive not only to the environmental but also to genetic perturbations associated with stress. The congruence of stress-induced and between-species patterns of variation in non-integrated traits suggests that stress-induced variation in these traits may play an important role in species divergence.
• Badyaev, A. V., & Hill, G. E. (2000). Evolution of sexual dichromatism: Contribution of carotenoid- versus melanin-based coloration. Biological Journal of the Linnean Society, 69(2), 153-172.
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  Abstract: In birds, carotenoid-based plumage coloration is more dependent on physical condition and foraging abilities and less constrained developmentally than is melanin-based coloration. Thus, female mate choice for honest signals should result in more intense sexual selection on carotenoid- than on melanin-based plumage coloration. Using variation in sexual dimorphism as an indirect measure of the intensity of sexual selection, we tested the prediction that variation in sexual dimorphism is driven more by change in carotenoid-based coloration between males and females than by change in melanin-based coloration. Examination of historical changes in carotenoid- versus melanin-based pigmentation in 126 extant species of Cardueline finches supported this prediction. We found that carotenoid-derived coloration changed more frequently among congeners than melanin-based coloration. In both sexes, increase in carotenoid-based coloration score, but not in melanin-based coloration score, was strongly associated with increase in sexual dichromatism. In addition, sexual dimorphism in carotenoid-based coloration contributed more to overall dichromatism than dimorphism in melanin-based plumage. Our results supported the hypothesis that melanin-based and carotenoid-based coloration have fundamentally different signal content and suggest that combining melanin-based and carotenoid-based coloration in comparative analyses is not appropriate. (C) 2000 The Linnean Society of London.
• Badyaev, A. V., & Hill, G. E. (2000). The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution, 54(5), 1784-1794.
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  PMID: 11108605;Abstract: Patterns of genetic variation and covariation strongly affect the rate and direction of evolutionary change by limiting the amount and form of genetic variation available to natural selection. We studied evolution of morphological variance-covariance structure among seven populations of house finches (Carpodacus mexicanus) with a known phylogenetic history. We examined the relationship between within- and among-population covariance structure and, in particular, tested the concordance between hierarchical changes in morphological variance-covariance structure and phylogenetic history of this species. We found that among-population morphological divergence in either males or females did not follow the within-population covariance patterns. Hierarchical patterns of similarity in morphological covariance matrices were not congruent with a priori defined historical pattern of population divergence. Both of these results point to the lack of proportionality in morphological covariance structure of finch populations, suggesting that random drift alone is unlikely to account for observed divergence. Furthermore, drift alone cannot explain the sex differences in within- and among-population covariance patterns or sex-specific patterns of evolution of covariance structure. Our results suggest that extensive among-population variation in sexual dimorphism in morphological covariance structure was produced by population differences in local selection pressures acting on each sex.
• Badyaev, A. V., & Martin, T. E. (2000). Individual variation in growth trajectories: Phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus). Journal of Evolutionary Biology, 13(2), 290-301.
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  Abstract: We studied patterns of growth in a recently established natural population of the house finch (Carpodacus mexicanus) to examine whether phenotypic and genetic covariation among age-specific trait values is likely to constrain morphological change favoured by selection acting on adults. We found variable patterns of allometric relationships during ontogeny, and documented relatively weak covariations among ages or among traits in individual growth trajectories. Frequent compensatory growth largely cancelled out the initial differences among nestlings, potentially enabling house finches to raise offspring under diverse and unpredictable environmental conditions. Moderate levels of additive genetic variance in morphological traits throughout ontogeny, and relatively low and fluctuating phenotypic and genetic covariation among ages imply strong potential for evolutionary change in morphological traits tinder selection. This conclusion is consistent with the profound population-level divergence in morphological patterns that accompanied very successful colonization of most of North America by the house finch over the last 50 years.
• Badyaev, A. V., & Martin, T. E. (2000). Sexual dimorphism in relation to current selection in the house finch. Evolution, 54(3), 987-997.
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  PMID: 10937271;Abstract: Sexual dimorphism is thought to have evolved in response to selection pressures that differ between males and females. Our aim in this study was to determine the role of current net selection in shaping and maintaining contemporary sexual dimorphism in a recently established population of the house finch (Carpodacus mexicanus) in Montana. We found strong differences between sexes in direction of selection on sexually dimorphic traits, significant heritabilities of these traits, and a close congruence between current selection and observed sexual dimorphism in Montana house finches. Strong directional selection on sexually dimorphic traits and similar intensities of selection in each sex suggested that sexual dimorphism arises from adaptive responses in males and females, with both sexes being far from their local fitness optimum. This pattern is expected when a recently established population experiences continuous immigration from ecologically distinct areas of a species range or as a result of widely fluctuating selection pressures, as found in our study. Strong and sexually dimorphic selection pressures on heritable morphological traits, in combination with low phenotypic and genetic covariation among these traits during growth, may have accounted for close congruence between current selection and observed sexual dimorphism in the house finch. This conclusion is consistent with the profound adaptive population divergence in sexual dimorphism that accompanied very successful colonization of most of the North America by the house finch over the last 50 years.
• Badyaev, A. V., Foresman, K. R., & Fernandes, M. V. (2000). Stress and developmental stability: Vegetation removal causes increased fluctuating asymmetry in shrews. Ecology, 81(2), 336-345.
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  Abstract: Environmental stress can increase phenotypic variation in populations by affecting developmental stability of individuals. While such increase in variation results from individual differences in ability to buffer stress, groups of individuals and different traits may have different sensitivity to stressful conditions. For example, the sex that is under stronger directional selection for faster growth may be more sensitive to stressful conditions during development. On an individual level, stress-induced variation in a trait may be related to the strength of stabilizing selection that acts on the trait. We experimentally examined sensitivity of mandibular development to stress in a free-living population of common Shrews (Sorex cinereus), a short-lived insectivore mammal with very limited dispersal and nearly continuous foraging activity. We found a strong increase in asymmetry in shrews born under stressful conditions. Increased asymmetry was associated with lower physiological condition in both control and stressed populations, although the effect of asymmetry on fitness was more pronounced under stressful conditions. Males' developmental stability was more sensitive to stressful conditions than developmental stability of females, suggesting that their apparently faster and more variable growth is more sensitive to stress than is growth of females. Mandible traits differed in their sensitivity to environmental changes. Preliminary results suggest that this differential sensitivity is proportional to the degree of developmental and functional morphological integration among mandibular traits.
• Badyaev, A. V., Hill, G. E., Stoehr, A. M., Nolan, P. M., & McGraw, K. J. (2000). The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection. Evolution, 54(6), 2134-2144.
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  PMID: 11209788;Abstract: Recent colonization of ecologically distinct areas in North America by the house finch (Carpodacus mexicanus) was accompanied by strong population divergence in sexual size dimorphism. Here we examined whether this divergence was produced by population differences in local selection pressures acting on each sex. In a long-term study of recently established populations in Alabama, Michigan, and Montana, we examined three selection episodes for each sex: selection for pairing success, overwinter survival, and within-season fecundity. Populations varied in intensity of these selection episodes, the contribution of each episode to the net selection, and in the targets of selection. Direction and intensity of selection strongly differed between sexes, and different selection episodes often favored opposite changes in morphological traits. In each population, current net selection for sexual dimorphism was highly concordant with observed sexual dimorphism - in each population, selection for dimorphism was the strongest on the most dimorphic traits. Strong directional selection on sexually dimorphic traits, and similar intensities of selection in both sexes, suggest that in each of the recently established populations, both males and females are far from their local fitness optimum, and that sexual dimorphism has arisen from adaptive responses in both sexes. Population differences in patterns of selection on dimorphism, combined with both low levels of ontogenetic integration in heritable sexually dimorphic traits and sexual dimorphism in growth patterns, may account for the close correspondence between dimorphism in selection and observed dimorphism in morphology across house finch populations.
• Badyaev, A. V. (1999). Nesting habitat and nesting success of eastern wild turkeys in the Arkansas Ozark highlands. NCASI Technical Bulletin, 17-.
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  Abstract: [The author] studied nesting habitat of the eastern wild turkey (Meleagris gallopavo silvestris) in the Arkansas Ozarks during the breeding seasons of 1992 and 1993. Hens selected cover with greater complexity and variability in habitat structure than was generally available. Vegetation in preferred cover types provided substantial concealment at 0-1 m height. Hens selected large patches of habitat (about 80 m in diameter) for nesting. Areas adjacent to nests had characteristics intermediate between nest and non-use sites. Open overstory at nest sites and dense understory adjacent to the nest-site areas were apparently used as cues in nest habitat selection early in spring. Parameters correlated with enhanced lateral and overhead concealment of the nest site contributed the most to discrimination between used and non-used sites. Successful and depredated nests were best discriminated when data were considered on a larger spatial scale. Visual obstruction of the nest at 0-1 m height and variable nesting habitat appearance contributed the most to avoiding nest predation. Vegetation characteristics at renest sites were more variable, resulting in habitat appearance more diverse than that of first nest sites. [The author] suggest[s] that nest predation influences habitat selection here and availability of suitable nesting habitat may be a limiting factor for wild turkey populations in the Arkansas Ozarks.
• Badyaev, A. V. (1998). Environmental stress and developmental stability in dentition of the yellowstone grizzly bears. Behavioral Ecology, 9(4), 339-344.
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  Abstract: Asymmetry in bilateral traits is often used to assess an individual's quality and stress resistance, but stress-induced variation in developmental stability is largely undocumented for free-living populations. Over many years, grizzly bears (Ursus arctos horribilis) extensively foraged around garbage dumps in Yellowstone National Park. Abrupt closure of these dumps 26 years ago was a severely stressful event and was followed by excessive mortality and a many-fold increase in grizzly home-range size. I examine how this stress affected developmental stability by comparing dentition of bears born before and after the dump closure. I predicted that (1) asymmetry in dentition should be greater in bears born after dump closure compared to before closure, and asymmetry in sexually selected canines should change more than nonsexually selected premolars following dump closure and (2) the relationship between tooth asymmetry and tooth size should change in the populations following the stressful events as compared with populations before stressful events. I found that developmental stability of canines, which are under directional sexual selection in males, was more responsive to stress compared to that of male premolars or female dentition (both under stabilizing selection), and, because of the increased cost of canine production, fewer animals were able to achieve both large size and symmetrical development of these teeth, and thus the slope of the relationship between fluctuating asymmetry and canine size increased. I conclude that stress appears to act as an honesty-reinforcement mechanism in sexual selection for symmetrical dentition.
• Badyaev, A. V., & Ghalambor, C. K. (1998). Does a trade-off exist between sexual ornamentation and ecological plasticity? Sexual dichromatism and occupied elevational range in finches. Oikos, 82(2), 319-324.
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  Abstract: Secondary sexual traits are thought to be costly to produce and maintain, and the allocation of energy to sexual traits could result in reduced investment in traits associated with growth and basic maintenance. It has been suggested that the trade-off between sexual traits and growth and maintenance traits should manifest itself in the correlation between development of sexual traits and resistance to environmental variability. Interspecifically, this hypothesis predicts that species with greater sexual ornamentation and dimorphism should be able to tolerate a narrower width of environmental condition compared to related species with less developed sexual traits. We tested this prediction by examining whether sexual dimorphism in cardueline finches was negatively associated with the width of elevational range occupied during breeding. We assumed that the range in elevations where breeding can occur represents a measure of tolerance of environmental variability. We found a positive rather than a negative relationship between breeding range and sexual dimorphism. Finches that were capable of breeding over a large range of elevations were also more dimorphic in plumage. Possible explanations for the observed relationship between sexual dichromatism and ecological breadth could include interspecific differences in food availability and foraging ability, as well as variation in energy required for baseline metabolism.
• Badyaev, A. V., Etges, W. J., Faust, J. D., & Martin, T. E. (1998). Fitness correlates of spur length and spur asymmetry in male wild turkeys. Journal of Animal Ecology, 67(6), 845-852.
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  Abstract: 1. Tarsal spurs play an important role in intrasexual competition for females among male wild turkeys (Meleagris gallopavo). Thus variation in spur development may have important fitness consequences. 2. Fitness correlates of spur development were studied in a free-living population of wild turkeys and it was found that heavier males and males with longer beards had longer spurs. Males that had longer spurs spent more time on display areas during the breeding season and less time moving among these areas compared to males with shorter spurs, independently of their body mass. 3. Otherwise ideally symmetrical spurs showed fluctuating asymmetry between left and right tarsi, the degree of absolute asymmetry decreased with spur length in adults, but not in subadults, and males that survived at least one winter had more symmetrical spurs compared to males that did not. 4. We conclude that if the ability to produce symmetrical spurs has a genetic basis, then spur length and spur asymmetry could reliably indicate individual quality and that these traits are under directional selection for increased size and symmetry in wild turkeys.
• Kupriyanova, E. K., & Badyaev, A. V. (1998). Ecological correlates of Arctic Serpulidae (Annelida, Polychaeta) distributions. Ophelia, 49(3), 181-193.
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  Abstract: Polychaetes are traditionally considered poor biogeographic indicators because they tend to show ecological rather than geographic fidelity in their distribution. We analyzed distributions of arctic Serpulidae from ecological and biogeographic perspectives. Habitat associations were studied by principal component, correspondence, cluster, and discriminant function analyses. Records for each site included depth, temperature, salinity and sediment type, with particle size analysis and notes of whether the sample also contained rocks or shells. Temperature and depth are shown to be major environmental factors controlling distributions. Substrate associations differed significantly among studied species and appeared to be determined by sedimentation tolerances of individual species. Bathymetrically, the arctic serpulid fauna mostly consists of lower sublittoral-upper bathyal and lower sublittoral-bathyal species. Clustering by habitat produced four groups: 1) deep- and cold-water species (Protis arctica, Hyalopomatus claparedii); 2) relatively warm-water species associated with hard sediments (Hydroides norvegicus, Serpula vermicularis, and Pomatoceros triqueter); 3) warm-water species associated with soft sediments (Ditrupa); 4) group with the highest habitat variability, associated to a larger degree with soft sediments (Filograna implexa, Placostegus tridentatus, Protula globifera and Protula tubularia). The fauna of arctic serpulids consists of North-Atlantic boreal forms with complete absence of Pacific elements. Both distribution ranges and habitat characteristics suggest that the fauna of arctic serpulids is formed by post-glacial Atlantic migrants penetrating into the Arctic with warm Atlantic currents, with the addition of deep-water relicts of the pre-glacial fauna.
• Badyaev, A. V. (1997). Altitudinal variation in sexual dimorphism: A new pattern and alternative hypotheses. Behavioral Ecology, 8(6), 675-690.
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  Abstract: The colder climate and disjunct distribution of nesting and foraging habitats at high elevations increases the necessity of biparental care for successful breeding in birds. If differences in parental investment between the sexes correlate with intensity of sexual selection, the intensity of sexual selection should covary with ecological factors associated with elevation. I used sexual dimorphism as an indirect measure of intensity of sexual selection and examined variation in sexual dimorphism in 126 extant species of cardueline finches. I controlled for phylogeny and potential confounding factors and tested the prediction that the extent of sexual dimorphism negatively covaries with elevation of breeding. As predicted, interspecific variation in sexual dimorphism was more strongly associated with changes in elevation than with habitat, nest dispersion and placement, and migratory status. Species occupying lower elevations were more sexually dimorphic in plumage than species at higher elevations. This variation was largely due to increased brightness of male plumage at lower elevations. I address possible explanations of this trend, which may include increased opportunities for extrapair fertilizations at lower elevations, an increase in the cost of secondary sexual trait production (i.e., molt) and maintenance at high elevations, and elevational variation in predation pressure.
• Badyaev, A. V. (1997). Avian life history variation along altitudinal gradients: An example with cardueline finches. Oecologia, 111(3), 365-374.
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  Abstract: Elevation has long been considered a major influence on the evolution of life-history traits. Most elevation-induced variation in life history traits has been attributed to changes in climate, duration of breeding season, predation, and food limitation. I use a phylogenetic approach to show that life histories are closely associated with breeding elevation in extant cardueline finches. Finches at high elevations had smaller clutches, fewer broods, and longer incubation periods. Neither food limitation nor nest predation appear to readily account for this strong elevational variation in cardueline life histories. However, juvenile survival may be greater at higher elevations as a result of prolonged parental care and shorter natal dispersal and can potentially compensate for reduced fecundity in high-elevation finches.
• Badyaev, A. V. (1997). Covariation between life history and sexually selected traits: An example with cardueline finches. Oikos, 80(1), 128-138.
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  Abstract: Traits associated with fecundity and survival are often subject to similar trade-offs because allocation of resources to one activity will limit the others. Such trade-offs have been proposed to account for sex-specific associations between life history and sexually selected traits. In this study I examined life history correlates of variation in sexual dimorphism in cardueline finches. These birds show strong variation in plumage sexual dichromatism. While this variation may reflect changes in intensity of sexual selection or cost of mate sampling, it could also be caused by differences in the costs of secondary sexual traits. I used path analysis to control for potential effects of breeding altitude, nest height, body size, migratory class, and phylogeny to show that variation in sexual dichromatism and plumage brightness in both sexes closely corresponded to variation in life history traits. Sexual dichromatism was negatively correlated with clutch size. Association between sexual ornamentation and fecundity was different for males and females. Male plumage brightness was negatively correlated with clutch size and numbers of broods, but female brightness was positively correlated with clutch size across extant cardueline finches. Nest height and altitude of breeding covaried with sexual dichromatism and with sexual ornamentation in both sexes. Association of sexual ornamentation with clutch size and numbers of broods was more similar between sexes in high-elevation species than in low-elevation species. In males, associations among plumage brightness and life history traits changed more with altitude compared to females. Similar selection pressures caused by equal sharing of parental care between sexes at higher altitudes may account for this pattern.
• Badyaev, A. V., & Leaf, E. S. (1997). Habitat associations of song characteristics in Phylloscopus and Hippolais warblers. Auk, 114(1), 40-46.
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  Abstract: Bird-song functions, such as mate attraction, species recognition, and territory defense, are closely linked to individual fitness. Thus, habitat characteristics that affect song transmission and degradation should exert a strong influence on the evolution of song attributes. Whereas different acoustic environments may influence the evolution of song characteristics, factors such as body size and evolutionary history of taxa are expected to constrain the amount of environmental variation in song properties. In the present study, we controlled for phylogeny and examined the effects of body mass and habitat structure on variation in song structure of 30 taxa of Phylloscopus and Hippolais warblers, which are a closely related group of birds that occupy a wide variety of habitats and show high variation in vocalizations Habitat structure was strongly correlated with temporal characteristics of songs but not with most of the frequency-related attributes that we measured. Only the highest frequencies of songs varied with habitat structure. As predicted, species occupying closed habitats avoided the use of rapidly modulated signals and had song structures that minimized reverberation. Body mass covaried significantly with most of the song attributes. Smaller species used higher frequencies and had more notes in their songs compared with larger species.
• Badyaev, A. V., & Faust, J. D. (1996). Nest site fidelity in female wild turkey: Potential causes and reproductive consequences. Condor, 98(3), 589-594.
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  Abstract: We studied nest site fidelity of female Wild Turkeys in the Arkansas Ozarks during 1992-94. Sixty-nine percent of surviving females returned to breed on their previous breeding areas. Older females had higher return rate compared to younger females. Females did not appear to base their return decision on the previous year nest success. Females that returned to their previous nesting areas laid larger clutches than females that did not return and nests of returned females survived longer than those of females that moved to new areas. Nest site fidelity did not associate with future reproductive success; nest success of females that returned and those that switched breeding areas was similar. Spring dispersal distance and size of prenesting ranges were similar between females that returned and females that moved to new areas between years. Females that nested in habitats that appeared to provide reduced protection from predation relocated in the following year independently of whether their previous nests actually were depredated. Increased social status and experience may account for correlation between habitat quality and breeding site fidelity.
• Badyaev, A. V., Etges, W. J., & Martin, T. E. (1996). Age-biased spring dispersal in male wild turkeys. Auk, 113(1), 240-242.
• Badyaev, A. V., Etges, W. J., & Martin, T. E. (1996). Ecological and behavioral correlates of variation in seasonal home ranges of wild turkeys. Journal of Wildlife Management, 60(1), 154-164.
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  Abstract: We examined the effects of habitat distribution, age, sex, and body mass on variation in seasonal home ranges of eastern wild turkeys (Meleagris gallopavo silvestris). During 1992-94 we obtained and analyzed 11,354 locations of 156 wild turkeys in the Arkansas Ozarks. In particular, we tested the prediction that home range size and seasonal range juxtaposition covary with social status and physiological condition of an individual. Participation in breeding, age, and body mass strongly influenced spring and summer range sizes and range use in both sexes. As predicted, adult wild turkeys had smaller home ranges during the breeding season and greater overlap among seasonal ranges than yearlings. Successful females had a higher probability of using their breeding area during fall and winter than unsuccessful females. Habitat availability and distribution and acorn harvest were significant correlates of winter range size and use for females. Spring and prenesting ranges of females in our study area were the largest reported for eastern wild turkeys. We attributed this pattern to high nest predation which might cause extensive nest site selection movements.
• Badyaev, A. V., Martin, T. E., & Etges, W. J. (1996). Habitat sampling and habitat selection by female Wild Turkeys: Ecological correlates and reproductive consequences. Auk, 113(3), 636-646.
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  Abstract: Habitat sampling can allow much more effective habitat selection for long-term activities such as nesting and may be directly linked to fitness. We studied the process of habitat sampling and selection in female Wild Turkeys (Meleagris gallopavo) in the Arkansas Ozarks. In particular, we tested the prediction that movements prior to selecting nesting habitat correlate with the quality of selected habitat. Our results supported the prediction that greater habitat sampling (as reflected by greater area covered prior to nesting) allows acquisition of better nesting habitat; greater movements were correlated with choice of better nesting sites with more cover that allow higher nest survival. Attributes of individual birds and habitat dispersion influenced movement patterns and access to quality habitats. In addition, extent of habitat sampling early in the season correlated with reproductive performance by affecting renesting. Distance between subsequent nest locations was inversely related to the movements early in the season and also depended upon length of incubation before nest predation. Females that sampled larger areas after depredation of their first nest and did so outside of their prenesting range were more successful than other females.
• Martin, T. E., & Badyaev, A. V. (1996). Sexual dichromatism in birds: Importance of nest predation and nest location for females versus males. Evolution, 50(6), 2454-2460.
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  Abstract: Examinations of variation in plumage dichromatism in birds have focused on male plumage brightness and largely neglected variation in female plumage brightness. Nest predation previously was concluded to constrain male brightness and thereby reduce dimorphism in ground-nesting birds based on an incorrect assumption that nest predation is greater for ground nests. Correlations of plumage brightness and dichromatism with nest predation have never been tested directly and we do so here with data for warblers (Parulinae) and finches (Carduelinae). We show that male plumage brightness varies among nest heights, but in a pattern that is not correlated with nest predation Female plumage brightness also varies among nest heights, but in a pattern that differs from males, and one in which variation in female plumage brightness was negatively correlated with nest predation. These results suggest that nest predation may place greater constraints on female than male plumage brightness, at least in taxa where only females incubate eggs and brood young. These results also show that female plumage patterns vary at least partly independently of male patterns and emphasize the need to include consideration of both female and male plumage variation in tests of plumage dimorphism. Plumage dimorphism differs between ground and off-ground nesters as previously described and, if anything, the relationship between plumage dimorphism and nest predation was positive rather than negative as previously argued.
• Badyaev, A. V. (1995). Nesting habitat and nesting success of eastern wild turkeys in the Arkansas ozark highlands. Condor, 97(1), 221-232.