Rick Michod

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Scholarly Contributions

Chapters

• Hanschen, E., Shelton, D. E., & Michod, R. E. (2015). Recent models on the evolution of cellular specialization: context, comparisons, and remaining questions. In Evolutionary Transitions to Multicellular Life(pp 165-188). Advances in Marine Genomics 2. Springer. Science+Business Media Dordrecht. doi:10.1007/978-94-017-9642-2_9
• Nedelcu, A., & Michod, R. E. (2011). Molecular mechanisms of life history trade-offs and the evolution of multicellular complexity in volvocalean green algae. In Mechanisms of Life History Evolution. The Genetics and Physiology of Life History Traits and Trade-Offs(pp 271-283). Oxford University Press.
• Michod, R. E. (2011). Sex and multicellularity as evolutionary transitions in individuality. In Major Transitions in Evolution Revisited(pp 169-199). Vienna Series in Theoretical Biology: MIT Press.
• Bernstein, H., Bernstein, C., & Michod, R. E. (2011). Meiosis as an Evolutionary Adaptation for DNA Repair. In DNA Repair(pp Chapter 19). InTech - Open Access Publisher, Slavka Krautzeka, Croatia.

Journals/Publications

• Davison, D., & Michod, R. (2023). Steps to individuality in biology and culture. Philosophical Transactions of the Royal Society B, 378(1872). doi:10.1098/rstb.2021.0407
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  Did human culture arise through an evolutionary transition in individuality (ETI)? To address this question, we examine the steps of biological ETIs to see how they could apply to the evolution of human culture. For concreteness, we illustrate the ETI stages using a well-studied example, the evolution of multicellularity in the volvocine algae. We then consider how those stages could apply to a cultural transition involving integrated groups of cultural traditions and the hominins that create and transmit traditions. We focus primarily on the early Pleistocene and examine hominin carnivory and the cultural change from Oldowan to Acheulean technology. We use Pan behaviour as an outgroup comparison. We summarize the important similarities and differences we find between ETI stages in the biological and cultural realms. As we are not cultural anthropologists, we may overlook or be mistaken in the processes we associate with each step. We hope that by clearly describing these steps to individuality and illustrating them with cultural principles and processes, other researchers may build upon our initial exercise. Our analysis supports the hypothesis that human culture has undergone an ETI beginning with a Pan-like ancestor, continuing during the Pleistocene, and culminating in modern human culture. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.
• Maliet, O., Shelton, D. E., & Michod, R. E. (2015). A model for the origin of group reproduction during the evolutionary transition to multicellularity. Biology letters, 11(6), 20150157.
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  During the evolution of multicellular organisms, the unit of selection and adaptation, the individual, changes from the single cell to the multicellular group. To become individuals, groups must evolve a group life cycle in which groups reproduce other groups. Investigations into the origin of group reproduction have faced a chicken-and-egg problem: traits related to reproduction at the group level often appear both to be a result of and a prerequisite for natural selection at the group level. With a focus on volvocine algae, we model the basic elements of the cell cycle and show how group reproduction can emerge through the coevolution of a life-history trait with a trait underpinning cell cycle change. Our model explains how events in the cell cycle become reordered to create a group life cycle through continuous change in the cell cycle trait, but only if the cell cycle trait can coevolve with the life-history trait. Explaining the origin of group reproduction helps us understand one of life's most familiar, yet fundamental, aspects-its hierarchical structure.
• Rashidi, A., Shelton, D. E., & Michod, R. E. (2015). A Darwinian approach to the origin of life cycles with group properties. Theoretical population biology, 102, 76-84.
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  A selective explanation for the evolution of multicellular organisms from unicellular ones requires knowledge of both selective pressures and factors affecting the response to selection. Understanding the response to selection is particularly challenging in the case of evolutionary transitions in individuality, because these transitions involve a shift in the very units of selection. We develop a conceptual framework in which three fundamental processes (growth, division, and splitting) are the scaffold for unicellular and multicellular life cycles alike. We (i) enumerate the possible ways in which these processes can be linked to create more complex life cycles, (ii) introduce three genes based on growth, division and splitting that, acting in concert, determine the architecture of the life cycles, and finally, (iii) study the evolution of the simplest five life cycles using a heuristic model of coupled ordinary differential equations in which mutations are allowed in the three genes. We demonstrate how changes in the regulation of three fundamental aspects of colonial form (cell size, colony size, and colony cell number) could lead unicellular life cycles to evolve into primitive multicellular life cycles with group properties. One interesting prediction of the model is that selection generally favors cycles with group level properties when intermediate body size is associated with lowest mortality. That is, a universal requirement for the evolution of group cycles in the model is that the size-mortality curve be U-shaped. Furthermore, growth must decelerate with size.
• Durand, P. M., Choudhury, R., Rashidi, A., & Michod, R. E. (2014). Programmed death in a unicellular organism has species-specific fitness effects. Biology Letters, 10(2).
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  Abstract: Programmed cell death (PCD) is an ancient phenomenon and its origin and maintenance in unicellular life is unclear. We report that programmed death provides differential fitness effects that are species specific in the model organism Chlamydomonas reinhardtii. Remarkably, PCD in this organism not only benefits others of the same species, but also has an inhibitory effect on the growth of other species. These data reveal that the fitness effects of PCD can depend upon genetic relatedness. © 2014 The Author(s) Published by the Royal Society.
• Hanschen, E. R., Ferris, P. J., & Michod, R. E. (2014). Early evolution of the genetic basis for soma in the volvocaceae. Evolution; international journal of organic evolution, 68(7), 2014-25.
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  To understand the hierarchy of life in evolutionary terms, we must explain why groups of one kind of individual, say cells, evolve into a new higher level individual, a multicellular organism. A fundamental step in this process is the division of labor into nonreproductive altruistic soma. The regA gene is critical for somatic differentiation in Volvox carteri, a multicellular species of volvocine algae. We report the sequence of regA-like genes and several syntenic markers from divergent species of Volvox. We show that regA evolved early in the volvocines and predict that lineages with and without soma descended from a regA-containing ancestor. We hypothesize an alternate evolutionary history of regA than the prevailing "proto-regA" hypothesis. The variation in presence of soma may be explained by multiple lineages independently evolving soma utilizing regA or alternate genetic pathways. Our prediction that the genetic basis for soma exists in species without somatic cells raises a number of questions, most fundamentally, under what conditions would species with the genetic potential for soma, and hence greater individuality, not evolve these traits. We conclude that the evolution of individuality in the volvocine algae is more complicated and labile than previously appreciated on theoretical grounds.
• Herron, M. D., Ghimire, S., Vinikoor, C. R., & Michod, R. E. (2014). Fitness trade-offs and developmental constraints in the evolution of soma: an experimental study in a volvocine alga. EVOLUTIONARY ECOLOGY RESEARCH, 16(3), 203-221.
• Michod, R. E. (2014). Group selection and group adaptation during a major evolutionary transition: insights from the evolution of multicellularity in the volvocine algae. Biological Theory, 9, 452-469.
• Shelton, D. E., & Michod, R. E. (2014). Levels of selection and the formal Darwinism project. Biology and Philosophy, 29(2), 217-224.
• Smith, D. R., Hamaji, T., Olson, B. J., Durand, P. M., Ferris, P., Michod, R. E., Featherston, J., Nozaki, H., & Keeling, P. J. (2013). Organelle genome complexity scales positively with organism size in volvocine green algae. Molecular Biology and Evolution, 30(4), 793-797.
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  PMID: 23300255;Abstract: It has been argued that for certain lineages, noncoding DNA expansion is a consequence of the increased random genetic drift associated with long-term escalations in organism size. But a lack of data has prevented the investigation of this hypothesis in most plastid-bearing protists. Here, using newly sequenced mitochondrial and plastid genomes, we explore the relationship between organelle DNA noncoding content and organism size within volvocine green algae. By looking at unicellular, colonial, and differentiated multicellular algae, we show that organelle DNA complexity scales positively with species size and cell number across the volvocine lineage. Moreover, silent-site genetic diversity data suggest that the volvocine species with the largest cell numbers and most bloated organelle genomes have the smallest effective population sizes. Together, these findings support the view that nonadaptive processes, like random genetic drift, promote the expansion of noncoding regions in organelle genomes. © 2013 The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
• Bernstein, H., Bernstein, C., & Michod, R. E. (2012). DNA repair as the primary adaptive function of sex in bacteria and eukaryotes. DNA Repair: New Research, 1-50.
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  Abstract: The essential feature of sex common to both bacteria and eukaryotes is information exchange (recombination) between two genomic DNA molecules derived from different individuals. In bacteria a naturally occurring sexual process termed transformation is characterized by transfer of DNA from one bacterium to another, followed by recombination between the resident DNA and the incoming DNA. In eukaryotes, the sexual cycle involves recombination between paired DNA molecules (chromosomes) in which the two DNA molecules are derived from two different parents. This process occurs in diploid cells during meiosis, and is followed by formation of haploid gametes. The fusion of gametes from different individuals to generate diploid progeny completes the eukaryotic sexual cycle. DNA damage appears to be a fundamental problem for life. Here, we present evidence for the view that the enzymatic machinery for carrying out recombination, during transformation in bacteria and meiosis in eukaryotes, is an adaptation for DNA repair. Both bacterial and eukaryotic cells, generally, contain repair enzymes that are adept at removing DNA damages. However there are limits to the capability of cells during ordinary cell divisions to repair their DNA. Damages causing loss of information in both DNA strands (double-strand damages) are particularly difficult to handle since they require information from a second homologous chromosome. A repair process referred to as homologous recombinational repair (HRR) appears designed to carry out repair of such double-strand damages.Evidence is presented for the hypothesis that sexual processes (i.e. transformation in bacteria and meiosis in eukaryotes) are maintained as evolutionary adaptations to facilitate HRR. In bacteria and microbial eukaryotes the problem of DNA damages is particularly acute during periods of stress, especially oxidative stress. It is during such stressful conditions that sex (which facilitates HRR) tends to occur in these facultatively sexual organisms. In multicellular eukaryotes, meiosis facilitates HRR and appears to be designed to protect against damages to the DNA of gametes, thus minimizing infertility and defective progeny.Another consequence of recombination during sex is increased genetic variation among progeny. Increased variation appears to have significant consequences at the population level over the long-term and is sometimes considered the primary adaptive function of sex. However, we present evidence that the machinery for sexual recombination is maintained primarily by the strong short-term advantage of passing relatively undamaged DNA from one generation to the next. The genetic variation that is generated appears to be a byproduct of HRR. © 2012 Nova Science Publishers, Inc. All rights reserved.
• Michod, R. E., & Durand, P. (2011). What is life and why, how and when did it begin?. Journal of Cosmology, 16, 7050-7055.
• Shelton, D. E., Desnitskiy, A. G., & Michod, R. E. (2012). Distributions of reproductive and somatic cell numbers in diverse Volvox (Chlorophyta) species. Evolutionary Ecology Research, 14(6), 707-727.
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  Abstract: Background: Volvox (Chlorophyta) asexual colonies consist of two kinds of cells: a large number of small somatic cells and a few large reproductive cells. The numbers of reproductive and somatic cells correspond directly to the major components of fitness - fecundity and viability, respectively. Volvox species display diverse patterns of development that give rise to the two cell types. Questions: For Volvox species under fixed conditions, do species differ with respect to the distribution of somatic and reproductive cell numbers in a population of asexual clones? Specifically, do they differ with respect to the dispersion of the distribution, i.e. with respect to their intrinsic variability? If so, are these differences related to major among-species developmental differences? Data description: For each of five Volvox species, we estimate the number of somatic and reproductive cells for 40 colonies and the number of reproductive cells for an additional 200 colonies. We sampled all colonies from growing, low-density, asexual populations under standard conditions. Search method: We compare the distribution of reproductive cell numbers to a Poisson distribution. We also compare the overall dispersion of reproductive cell number among species by calculating the coefficient of variation (CV). We compare the bivariate (reproductive and somatic cell) dataset to simulated datasets produced from a simple model of cell-type specification with intrinsic variability and colony size variation. This allows us to roughly estimate the level of intrinsic variability that is most consistent with our observed bivariate data (given an unknown level of size variation). Conclusions: The overall variability (CV) in reproductive cell number is high in Volvox compared with more complex organisms. Volvox species show differences in reproductive cell number CV that were not clearly related to development, as currently understood. If we used the bivariate data and tried to account for the effects of colony size variation, we found that the species that have fast embryonic divisions and asymmetric divisions have substantially higher intrinsic variability than the species that have slow divisions and no asymmetric divisions. Under our culture conditions, the Poisson distribution is a good description of intrinsic variability in reproductive cell number for some but not all Volvox species. © 2012 Deborah E. Shelton.
• Abbot, P., Abe, J., Alcock, J., Alizon, S., A., J., Andersson, M., Andre, J., Baalen, M. V., Balloux, F., Balshine, S., Barton, N., Beukeboom, L. W., Biernaskie, J. M., Bilde, T., Borgia, G., Breed, M., Brown, S., Bshary, R., Buckling, A., , Burley, N. T., et al. (2011). Inclusive fitness theory and eusociality. Nature, 471(7339), e1-e4.
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  PMID: 21430721;PMCID: PMC3836173;
• Durand, P. M., Rashidi, A., & Michod, R. E. (2011). How an organism dies affects the fitness of its neighbors. The American naturalist, 177(2), 224-32.
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  Programmed cell death (PCD), a genetically regulated cell suicide program, is ubiquitous in the living world. In contrast to multicellular organisms, in which cells cooperate for the good of the organism, in unicells the cell is the organism and PCD presents a fundamental evolutionary problem. Why should an organism actively kill itself as opposed to dying in a nonprogrammed way? Proposed arguments vary from PCD in unicells being maladaptive to the assumption that it is an extreme form of altruism. To test whether PCD could be beneficial to nearby cells, we induced programmed and nonprogrammed death in the unicellular green alga Chlamydomonas reinhardtii. Cellular contents liberated during non-PCD are detrimental to others, while the contents released during PCD are beneficial. The number of cells in growing cultures was used to measure fitness. Thermostability studies revealed that the beneficial effect of the PCD supernatant most likely involves simple heat-stable biomolecules. Non-PCD supernatant contains heat-sensitive molecules like cellular proteases and chlorophyll. These data indicate that the mode of death affects the origin and maintenance of PCD. The way in which an organism dies can have beneficial or deleterious effects on the fitness of its neighbors.
• Ferriere, R., & Michod, R. E. (2011). Inclusive fitness in evolution. Nature, 471(7339), e6-e8.
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  PMID: 21430724;
• Michod, R. (2011). Diversity in the Epistemology Group: Ernst von Glasersfeld and the Question of Adaptation. CONSTRUCTIVIST FOUNDATIONS, 6(2), 162-163.
• Solari, C. A., Drescher, K., Ganguly, S., Kessler, J. O., Michod, R. E., & Goldstein, R. E. (2011). Flagellar phenotypic plasticity in volvocalean algae correlates with Péclet number. Journal of the Royal Society Interface, 8(63), 1409-1417.
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  PMID: 21367778;PMCID: PMC3163421;Abstract: Flagella-generated fluid stirring has been suggested to enhance nutrient uptake for sufficiently large micro-organisms, and to have played a role in evolutionary transitions to multicellularity. A corollary to this predicted size-dependent benefit is a propensity for phenotypic plasticity in the flow-generating mechanism to appear in large species under nutrient deprivation. We examined four species of volvocalean algae whose radii and flow speeds differ greatly, with Péclet numbers (Pe) separated by several orders of magnitude. Populations of unicellular Chlamydomonas reinhardtii and one- to eight-celled Gonium pectorale (Pe ∼ 0.1-1) and multicellular Volvox carteri and Volvox barberi (Pe ∼ 100) were grown in diluted and undiluted media. For C. reinhardtii and G. pectorale, decreasing the nutrient concentration resulted in smaller cells, but had no effect on flagellar length and propulsion force. In contrast, these conditions induced Volvox colonies to grow larger and increase their flagellar length, separating the somatic cells further. Detailed studies on V. carteri found that the opposing effects of increasing beating force and flagellar spacing balance, so the fluid speed across the colony surface remains unchanged between nutrient conditions. These results lend further support to the hypothesized link between the Péclet number, nutrient uptake and the evolution of biological complexity in the Volvocales. © 2011 The Royal Society.
• Durand, P. M., & Michod, R. E. (2010). Genomics in the light of evolutionary transitions. Evolution; international journal of organic evolution, 64(6), 1533-40.
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  Molecular biology has entrenched the gene as the basic hereditary unit and genomes are often considered little more than collections of genes. However, new concepts and genomic data have emerged, which suggest that the genome has a unique place in the hierarchy of life. Despite this, a framework for the genome as a major evolutionary transition has not been fully developed. Instead, genome origin and evolution are frequently considered as a series of neutral or nonadaptive events. In this article, we argue for a Darwinian multilevel selection interpretation for the origin of the genome. We base our arguments on the multilevel selection theory of hypercycles of cooperative interacting genes and predictions that gene-level trade-offs in viability and reproduction can help drive evolutionary transitions. We consider genomic data involving mobile genetic elements as a test case of our view. A new concept of the genome as a discrete evolutionary unit emerges and the gene-genome juncture is positioned as a major evolutionary transition in individuality. This framework offers a fresh perspective on the origin of macromolecular life and sets the scene for a new, emerging line of inquiry--the evolutionary ecology of the genome.
• Durand, P. M., & Michod, R. E. (2010). Genomics in the light of evolutionary transitions. Evolution, 64(6), 1533-1540.
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  PMID: 19930450;Abstract: Molecular biology has entrenched the gene as the basic hereditary unit and genomes are often considered little more than collections of genes. However, new concepts and genomic data have emerged, which suggest that the genome has a unique place in the hierarchy of life. Despite this, a framework for the genome as a major evolutionary transition has not been fully developed. Instead, genome origin and evolution are frequently considered as a series of neutral or nonadaptive events. In this article, we argue for a Darwinian multilevel selection interpretation for the origin of the genome. We base our arguments on the multilevel selection theory of hypercycles of cooperative interacting genes and predictions that gene-level trade-offs in viability and reproduction can help drive evolutionary transitions. We consider genomic data involving mobile genetic elements as a test case of our view. A new concept of the genome as a discrete evolutionary unit emerges and the gene-genome juncture is positioned as a major evolutionary transition in individuality. This framework offers a fresh perspective on the origin of macromolecular life and sets the scene for a new, emerging line of inquiry-the evolutionary ecology of the genome. © 2010 The Author(s). Journal compilation © 2010 The Society for the Study of Evolution.
• HOELZER, M., & MICHOD, R. (2010). DNA-REPAIR AND THE EVOLUTION OF TRANSFORMATION IN BACILLUS-SUBTILIS .3. SEX WITH DAMAGED DNA. GENETICS, 128(2), 215-223.
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  Natural genetic transformation in the bacterium Bacillus subtilis provides an experimental system for studying the evolutionary function of sexual recombination. The repair hypothesis proposes that during transformation the exogenous DNA taken up by cells is used as template for recombinational repair of damages in the recipient cell's genome. Earlier results demonstrated that the population density of transformed cells (i.e., sexual cells) increases, relative to nontransformed cells (primarily asexual cells), with increasing dosage of ultraviolet irradiation, provided that the cells are transformed with undamaged homologous DNA after they have become damaged. In nature, however, donor DNA for transformation is likely to come from cells that are as damaged as the recipient cells. In order to better simulate the effects of transformation in natural populations we conducted similar experiments as those just described using damaged donor DNA. We document in this report that transformants continue to increase in relative density even if they are transformed with damaged donor DNA. These results suggest that sites of transformation are often damaged sites in the recipient cell's genome.
• Herron, M. D., & Michod, R. E. (2010). Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin's eye. EVOLUTION, 62(2), 436-451.
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  The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation-conflict-conflict mediation cycles as predicted by multilevel selection theory. one such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.
• Herron, M. D., Desnitskiy, A. G., & Michod, R. E. (2010). Evolution of developmental programs in Volvox (Chlorophyta). Journal of Phycology, 46(2), 316-324.
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  Abstract: The volvocine green algal genus Volvox includes ∼20 species with diverse sizes (in terms of both diameter and cell number), morphologies, and developmental programs. Two suites of characters are shared among distantly related lineages within Volvox. The traits characteristic of all species of Volvox-large (>500) numbers of small somatic cells, much smaller numbers of reproductive cells, and oogamy in sexual reproduction-have three or possibly four separate origins. In addition, some species have evolved a suite of developmental characters that differs from the ancestral developmental program. Most multicellular volvocine algae, including some species of Volvox, share an unusual pattern of cell division known as palintomy or multiple fission. Asexual reproductive cells (gonidia) grow up to many times their initial size and then divide several times in rapid succession, with little or no growth between divisions. Three separate Volvox lineages have evolved a reduced form of palintomy in which reproductive cells are small and grow between cell divisions. In each case, these changes are accompanied by a reduction in the rate of cell division and by a requirement of light for cell division to occur. Thus, two suites of characters-those characteristic of all Volvox species and those related to reduced palintomy-have each evolved convergently or in parallel in lineages that diverged at least 175 million years ago (mya). © 2010 Phycological Society of America.
• MICHOD, R. (2010). WHATS LOVE GOT TO DO WITH IT - THE SOLUTION TO ONE OF EVOLUTIONS GREATEST RIDDLES. SCIENCES-NEW YORK, 29(3), 22-28.
• Roze, D., & Michod, R. E. (2010). Deleterious mutations and selection for sex in finite diploid populations. Genetics, 184(4), 1095-1112.
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  PMID: 20083613;PMCID: PMC2865910;Abstract: In diploid populations, indirect benefits of sex may stem from segregation and recombination. Although it has been recognized that finite population size is an important component of selection for recombination, its effects on selection for segregation have been somewhat less studied. In this article, we develop analytical two- and three-locus models to study the effect of recurrent deleterious mutations on a modifier gene increasing sex, in a finite diploid population. The model also incorporates effects of mitotic recombination, causing loss of heterozygosity (LOH). Predictions are tested using multilocus simulations representing deleterious mutations occurring at a large number of loci. The model and simulations show that excess of heterozygosity generated by finite population size is an important component of selection for sex, favoring segregation when deleterious alleles are nearly additive to dominant. Furthermore, sex tends to break correlations in homozygosity among selected loci, which disfavors sex when deleterious alleles are either recessive or dominant. As a result, we find that it is difficult to maintain costly sex when deleterious alleles are recessive. LOH tends to favor sex when deleterious mutations are recessive, but the effect is relatively weak for rates of LOH corresponding to current estimates (of the order 10-4-10 -5). Copyright © 2010 by the Genetics Society of America.
• Roze, D., & Michod, R. E. (2010). Deleterious mutations and selection for sex in finite diploid populations. Genetics, 184(4), 1095-112.
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  In diploid populations, indirect benefits of sex may stem from segregation and recombination. Although it has been recognized that finite population size is an important component of selection for recombination, its effects on selection for segregation have been somewhat less studied. In this article, we develop analytical two- and three-locus models to study the effect of recurrent deleterious mutations on a modifier gene increasing sex, in a finite diploid population. The model also incorporates effects of mitotic recombination, causing loss of heterozygosity (LOH). Predictions are tested using multilocus simulations representing deleterious mutations occurring at a large number of loci. The model and simulations show that excess of heterozygosity generated by finite population size is an important component of selection for sex, favoring segregation when deleterious alleles are nearly additive to dominant. Furthermore, sex tends to break correlations in homozygosity among selected loci, which disfavors sex when deleterious alleles are either recessive or dominant. As a result, we find that it is difficult to maintain costly sex when deleterious alleles are recessive. LOH tends to favor sex when deleterious mutations are recessive, but the effect is relatively weak for rates of LOH corresponding to current estimates (of the order 10(-4)-10(-5)).
• Herron, M. D., Hackett, J. D., Aylward, F. O., & Michod, R. E. (2009). Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3254-3258.
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  PMID: 19223580;PMCID: PMC2651347;Abstract: Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50-75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.
• Herron, M. D., Hackett, J. D., Aylward, F. O., & Michod, R. E. (2009). Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3254-8.
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  Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50-75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.
• Michod, R. (2009). Evolution of the individual. AMERICAN NATURALIST, 150, S5-S21.
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  This article studies the transition in evolution from single cells to multicellular organisms as a case study in the origin of individuality. The issues considered are applicable to all major transitions in the units of selection that involve the emergence of cooperation and the regulation of conflict. Explicit genetic models of mutation and selection both within and between organisms are studied. Cooperation among cells increases when the fitness covariance at the level of the organism overcomes within-organism change toward defection. Selection and mutation during development generate significant levels of within-organism variation and lead to variation in organism fitness at equilibrium. This variation selects for germ-line modifiers and other mediators of within-organism conflict, increasing the heritability of fitness at the organism level. The evolution of these modifiers is the first new function at the emerging organism level and a necessary component of the evolution of individuality.
• Herron, M. D., & Michod, R. E. (2008). Evolution of complexity in the volvocine algae: Transitions in individuality through Darwin's eye. Evolution, 62(2), 436-451.
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  PMID: 18031303;Abstract: The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation-conflict-conflict mediation cycles as predicted by multilevel selection theory. One such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress. © 2007 The Author(s).
• Herron, M. D., & Michod, R. E. (2008). Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye. Evolution; international journal of organic evolution, 62(2), 436-51.
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  The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation-conflict-conflict mediation cycles as predicted by multilevel selection theory. One such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.
• Michod, R. E., Bernstein, H., & Nedelcu, A. M. (2008). Adaptive value of sex in microbial pathogens. Infection, Genetics and Evolution, 8(3), 267-285.
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  PMID: 18295550;Abstract: Explaining the adaptive value of sex is one of the great outstanding problems in biology. The challenge comes from the difficulty in identifying the benefits provided by sex, which must outweigh the substantial costs of sex. Here, we consider the adaptive value of sex in viruses, bacteria and fungi, and particularly the information available on the adaptive role of sex in pathogenic microorganisms. Our general theme is that the varied aspects of sex in pathogens illustrate the varied issues surrounding the evolution of sex generally. These include, the benefits of sex (in the short- and long-term), as well as the costs of sex (both to the host and to the pathogen). For the benefits of sex (that is, its adaptive value), we consider three hypotheses: (i) sex provides for effective and efficient recombinational repair of DNA damages, (ii) sex provides DNA for food, and (iii) sex produces variation and reduces genetic associations among alleles under selection. Although the evolution of sex in microbial pathogens illustrates these general issues, our paper is not a general review of theories for the evolution of sex in all organisms. Rather, we focus on the adaptive value of sex in microbial pathogens and conclude that in terms of short-term benefits, the DNA repair hypothesis has the most support and is the most generally applicable hypothesis in this group. In particular, recombinational repair of DNA damages may substantially benefit pathogens when challenged by the oxidative defenses of the host. However, in the long-term, sex may help get rid of mutations, increase the rate of adaptation of the population, and, in pathogens, may infrequently create new infective strains. An additional general issue about sex illustrated by pathogens is that some of the most interesting consequences of sex are not necessarily the reasons for which sex evolved. For example, antibiotic resistance may be transferred by bacterial sex, but this transfer is probably not the reason sex evolved in bacteria. © 2008 Elsevier B.V. All rights reserved.
• Michod, R. E., Bernstein, H., & Nedelcu, A. M. (2008). Adaptive value of sex in microbial pathogens. Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, 8(3), 267-85.
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  Explaining the adaptive value of sex is one of the great outstanding problems in biology. The challenge comes from the difficulty in identifying the benefits provided by sex, which must outweigh the substantial costs of sex. Here, we consider the adaptive value of sex in viruses, bacteria and fungi, and particularly the information available on the adaptive role of sex in pathogenic microorganisms. Our general theme is that the varied aspects of sex in pathogens illustrate the varied issues surrounding the evolution of sex generally. These include, the benefits of sex (in the short- and long-term), as well as the costs of sex (both to the host and to the pathogen). For the benefits of sex (that is, its adaptive value), we consider three hypotheses: (i) sex provides for effective and efficient recombinational repair of DNA damages, (ii) sex provides DNA for food, and (iii) sex produces variation and reduces genetic associations among alleles under selection. Although the evolution of sex in microbial pathogens illustrates these general issues, our paper is not a general review of theories for the evolution of sex in all organisms. Rather, we focus on the adaptive value of sex in microbial pathogens and conclude that in terms of short-term benefits, the DNA repair hypothesis has the most support and is the most generally applicable hypothesis in this group. In particular, recombinational repair of DNA damages may substantially benefit pathogens when challenged by the oxidative defenses of the host. However, in the long-term, sex may help get rid of mutations, increase the rate of adaptation of the population, and, in pathogens, may infrequently create new infective strains. An additional general issue about sex illustrated by pathogens is that some of the most interesting consequences of sex are not necessarily the reasons for which sex evolved. For example, antibiotic resistance may be transferred by bacterial sex, but this transfer is probably not the reason sex evolved in bacteria.
• Roze, D., & Michod, R. E. (2008). Deleterious Mutations and Selection for Sex in Finite Diploid Populations. GENETICS, 184(4), 1095-U396.
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  In diploid populations, indirect benefits of sex may stem from segregation and recombination. Although it has been recognized that finite population size is an important component of selection for recombination, its effects on selection for segregation have been somewhat less studied. In this article, we develop analytical two-and three-locus models to study the effect of recurrent deleterious mutations on a modifier gene increasing sex, in a finite diploid population. The model also incorporates effects of mitotic recombination, causing loss of heterozygosity (LOH). Predictions are tested using multilocus simulations representing deleterious mutations occurring at a large number of loci. The model and simulations show that excess of heterozygosity generated by finite population size is an important component of selection for sex, favoring segregation when deleterious alleles are nearly additive to dominant. Furthermore, sex tends to break correlations in homozygosity among selected loci, which disfavors sex when deleterious alleles are either recessive or dominant. As a result, we find that it is difficult to maintain costly sex when deleterious alleles are recessive. LOH tends to favor sex when deleterious mutations are recessive, but the effect is relatively weak for rates of LOH corresponding to current estimates (of the order 10 (4)-10 (5)).
• Solari, C. A., Michod, R. E., & Goldstein, R. E. (2008). Volvox barberi, the fastest swimmer of the Volvocales (Chlorophyceae). Journal of Phycology, 44(6), 1395-1398.
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  Abstract: Volvox barberi W. Shaw is a volvocalean green alga composed of biflagellated cells. Vovocales with 16 cells or more form spherical colonies, and their largest members have germ-soma separation (all species in the genus Volvox). V. barberi is the largest Volvox species recorded in terms of cell number (10,000-50,000 cells) and has the highest somatic to reproductive cell ratio (S/R). Since they are negatively buoyant, Volvocales need flagellar beating to avoid sinking and to reach light and nutrients. We measured V. barberi swimming speed and total swimming force. V. barberi swimming speeds are the highest recorded so far for volvocine algae (∼600 μm·s -1). With this speed, V. barberi colonies have the potential to perform daily vertical migrations in the water column at speeds of 2-3 m·h-1, consistent with what has been reported about Volvox populations in the wild. Moreover, V. barberi data fit well in the scaling relationships derived with the other smaller Volvox species, namely, that the upward swimming speed Vup ∝ N 0.28 and the total swimming force FS ∝ N 0.77 (N = colony cell number). These allometric relationships have been important supporting evidence for reaching the conclusion that as size increases, colonies have to invest in cell specialization and increase their S/R to increase their motility capabilities to stay afloat and motile. © 2008 Phycological Society of America.
• HOPF, F., MICHOD, R., & SANDERSON, M. (2007). THE EFFECT OF THE REPRODUCTIVE-SYSTEM ON MUTATION LOAD. THEORETICAL POPULATION BIOLOGY, 33(3), 243-265.
• Michod, R. E. (2007). Evolution of individuality during the transition from unicellular to multicellular life. Proceedings of the National Academy of Sciences of the United States of America, 104 Suppl 1, 8613-8.
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  Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.
• Michod, R. E. (2007). Evolution of individuality during the transition from unicellular to multicellular life. Proceedings of the National Academy of Sciences of the United States of America, 104(SUPPL. 1), 8613-8618.
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  PMID: 17494748;PMCID: PMC1876437;Abstract: Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals. © 2007 by The National Academy of Sciences of the USA.
• BERNSTEIN, H., BYERLY, H., HOPF, F., & MICHOD, R. (2006). SEX AND THE EMERGENCE OF SPECIES. JOURNAL OF THEORETICAL BIOLOGY, 117(4), 665-690.
• Michod, R. (2006). Cooperation and conflict in the evolution of individuality .1. Multilevel selection of the organism. AMERICAN NATURALIST, 149(4), 607-645.
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  This article studies the transition in evolution from cells to multicellular organisms. The issues considered are applicable to all major transitions in the units of evolution that share two themes: the emergence of cooperation and the regulation of conflict among the lower-level units, in this case, cells. Explicit genetic models of mutation and selection both within and between organisms are studied in sexual and asexual haploid and diploid organisms without a germ line. The results may be understood in terms of the differing opportunities for within-and between-organism selection under the different reproductive modes and parameter values. Cooperation among cells increases when the fitness covariance at the level of the organism overcomes within-organism change toward defecting cells. Selection and mutation during development generate significant levels of within-organism variation and lead to significant variation in organism fitness at equilibrium. The levels of cooperativity attained can be low, even with reproduction passing through a single-cell zygote stage and the high kinship that entails. Sex serves to maintain higher levels of cooperation and lower levels of within-organism change. Fixed size may help organisms reduce conflict among cells.
• Michod, R. E. (2006). The group covariance effect and fitness trade-offs during evolutionary transitions in individuality. Proceedings of the National Academy of Sciences of the United States of America, 103(24), 9113-9117.
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  PMID: 16751277;PMCID: PMC1482575;Abstract: Transforming our understanding of life is the realization that evolution occurs not only among individuals within populations but also through the integration of groups of preexisting individuals into a new higher-level individual, that is, through evolutionary transitions in individuality. During evolutionary transitions (such as during the origin of gene networks, bacteria-like cells, eukaryotic cells, multicellular organisms, and societies), fitness must be reorganized; specifically, it must be transferred from the lower- to the higher-level units and partitioned among the lower-level units that specialize in the fitness components of the new higher-level individual. This paper studies the role of fitness trade-offs in fitness reorganization, the evolution of cooperation, and the conversion of a group into a new individual during the origin of multicellular life. Specifically, this study shows that the fitness of the group is augmented over the average fitness of its members according to a covariance effect. This covariance effect appears to be one of the first emergent properties of the group and a general aspect of groups with multiplicative properties that are themselves averages of properties of lower-level units. The covariance effect allows groups to break through the constraints that govern their members, and this effect likely applies to group dynamics in other fields. © 2006 by The National Academy of Sciences of the USA.
• Michod, R. E., & Herron, M. D. (2006). Cooperation and conflict during evolutionary transitions in individuality. Journal of Evolutionary Biology, 19(5), 1406-1409.
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  PMID: 16910968;
• Michod, R. E., Viossat, Y., Solari, C. A., Hurand, M., & Nedelcu, A. M. (2006). Life-history evolution and the origin of multicellularity. Journal of Theoretical Biology, 239(2), 257-272.
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  PMID: 16288782;Abstract: The fitness of an evolutionary individual can be understood in terms of its two basic components: survival and reproduction. As embodied in current theory, trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. Here, we argue that the evolution of germ-soma specialization and the emergence of individuality at a new higher level during the transition from unicellular to multicellular organisms are also consequences of trade-offs between the two components of fitness - survival and reproduction. The models presented here explore fitness trade-offs at both the cell and group levels during the unicellular-multicellular transition. When the two components of fitness negatively covary at the lower level there is an enhanced fitness at the group level equal to the covariance of components at the lower level. We show that the group fitness trade-offs are initially determined by the cell level trade-offs. However, as the transition proceeds to multicellularity, the group level trade-offs depart from the cell level ones, because certain fitness advantages of cell specialization may be realized only by the group. The curvature of the trade-off between fitness components is a basic issue in life-history theory and we predict that this curvature is concave in single-celled organisms but becomes increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the initial cost of reproduction to survival which increases as group size increases. To illustrate the principles and conclusions of the model, we consider aspects of the biology of the volvocine green algae, which contain both unicellular and multicellular members. © 2005 Elsevier Ltd. All rights reserved.
• Nedelcu, A. M., & Michod, R. E. (2006). The evolutionary origin of an altruistic gene. Molecular Biology and Evolution, 23(8), 1460-1464.
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  PMID: 16720695;Abstract: Although the conditions favoring altruism are being increasingly understood, the evolutionary origins of the genetic basis for this behavior remain elusive. Here, we show that reproductive altruism (i.e., a sterile soma) in the multicellular green alga, Volvox carteri, evolved via the co-option of a life-history gene whose expression in the unicellular ancestor was conditioned on an environmental cue (as an adaptive strategy to enhance survival at an immediate cost to reproduction) through shifting its expression from a temporal (environmentally induced) into a spatial (developmental) context. The gene belongs to a diverged and structurally heterogeneous multigene family sharing a SAND-like domain (a DNA-binding module involved in gene transcription regulation). To our knowledge, this is the first example of a social gene specifically associated with reproductive altruism, whose origin can be traced back to a solitary ancestor. These findings complement recent proposals that the differentiation of sterile castes in social insects involved the co-option of regulatory networks that control sequential shifts between phases in the life cycle of solitary insects. © The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved.
• Nedelcu, A., Marcu, O., & Michod, R. (2006). Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 271(1548), 1591-1596.
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  Organisms are constantly subjected to factors that can alter the cellular redox balance and result in the formation of a series of highly reactive molecules known as reactive oxygen species (ROS). As ROS can be damaging to biological structures, cells evolved a series of mechanisms (e.g. cell-cycle arrest, programmed cell death) to respond to high levels of ROS (i.e. oxidative stress). Recently, we presented evidence that in a facultatively sexual lineage-the multicellular green alga Volvox carteri-sex is an additional response to increased levels of stress, and probably ROS and DNA damage. Here we show that, in V. carteri, (i) sex is triggered by an approximately twofold increase in the level of cellular ROS (induced either by the natural sex-inducing stress, namely heat, or by blocking the mitochondrial electron transport chain with antimycin A), and (ii) ROS are responsible for the activation of sex genes. As most types of stress result in the overproduction of ROS, we believe that our findings will prove to extend to other facultatively sexual lineages, which could be indicative of the ancestral role of sex as an adaptive response to stress and ROS-induced DNA damage.
• Solari, C. A., Ganguly, S., Kessler, J. O., Michod, R. E., & Goldstein, R. E. (2006). Multicellularity and the functional interdependence of motility and molecular transport. Proceedings of the National Academy of Sciences of the United States of America, 103(5), 1353-1358.
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  PMID: 16421211;PMCID: PMC1360517;Abstract: Benefits, costs, and requirements accompany the transition from motile totipotent unicellular organisms to multicellular organisms having cells specialized into reproductive (germ) and vegetative (sterile soma) functions such as motility. In flagellated colonial organisms such as the volvocalean green algae, organized beating by the somatic cells' flagella yields propulsion important in phototaxis and chemotaxis. It has not been generally appreciated that for the larger colonies flagellar stirring of boundary layers and remote transport are fundamental for maintaining a sufficient rate of metabolite turnover, one not attainable by diffusive transport alone. Here, we describe experiments that quantify the role of advective dynamics in enhancing productivity in germ soma-differentiated colonies. First, experiments with suspended deflagellated colonies of Volvox carteri show that forced advection improves productivity. Second, particle imaging velocimetry of fluid motion around colonies immobilized by micropipette aspiration reveals flow fields with very large characteristic velocities U extending to length scales exceeding the colony radius R. For a typical metabolite diffusion constant D, the associated Peclet number Pe = 2UR/D 3 ≫ 1, indicative of the dominance of advection over diffusion, with striking augmentation at the cell division stage. Near the colony surface, flows generated by flagella can be chaotic, exhibiting mixing due to stretching and folding. These results imply that hydrodynamic transport external to colonies provides a crucial boundary condition, a source for supplying internal diffusional dynamics. © 2006 by The National Academy of Sciences of the USA.
• Solari, C. A., Kessler, J. O., & Michod, R. E. (2006). A hydrodynamics approach to the evolution of multicellularity: Flagellar motility and germ-soma differentiation in volvocalean green algae. American Naturalist, 167(4), 537-554.
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  PMID: 16670996;Abstract: During the unicellular-multicellular transition, there are opportunities and costs associated with larger size. We argue that germ-soma separation evolved to counteract the increasing costs and requirements of larger multicellular colonies. Volvocalean green algae are uniquely suited for studying this transition because they range from unicells to multicellular individuals with germ-soma separation. Because Volvocales need flagellar beating for movement and to avoid sinking, their motility is modeled and analyzed experimentally using standard hydrodynamics. We provide comparative hydrodynamic data of an algal lineage composed of organisms of different sizes and degrees of complexity. In agreement with and extending the insights of Koufopanou, we show that the increase in cell specialization as colony size increases can be explained in terms of increased motility requirements. First, as colony size increases, soma must evolve, the somatic-to-reproductive cell ratio increasing to keep colonies buoyant and motile. Second, increased germ-soma specialization in larger colonies increases motility capabilities because internalization of nonflagellated germ cells decreases colony drag. Third, our analysis yields a limiting maximum size of the volvocalean spheroid that agrees with the sizes of the largest species known. Finally, the different colony designs in Volvocales reflect the trade-offs between reproduction, colony size, and motility. © 2006 by The University of Chicago.
• Solari, C. A., Michod, R. E., & Goldstein, R. E. (2006). VOLVOX BARBERI, THE FASTEST SWIMMER OF THE VOLVOCALES (CHLOROPHYCEAE). JOURNAL OF PHYCOLOGY, 44(6), 1395-1398.
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  Volvox barberi W. Shaw is a volvocalean green alga composed of biflagellated cells. Vovocales with 16 cells or more form spherical colonies, and their largest members have germ-soma separation (all species in the genus Volvox). V. barberi is the largest Volvox species recorded in terms of cell number (10,000-50,000 cells) and has the highest somatic to reproductive cell ratio (S/R). Since they are negatively buoyant, Volvocales need flagellar beating to avoid sinking and to reach light and nutrients. We measured V. barberi swimming speed and total swimming force. V. barberi swimming speeds are the highest recorded so far for volvocine algae (similar to 600 mu m . s(-1)). With this speed, V. barberi colonies have the potential to perform daily vertical migrations in the water column at speeds of 2-3 m . h(-1), consistent with what has been reported about Volvox populations in the wild. Moreover, V. barberi data fit well in the scaling relationships derived with the other smaller Volvox species, namely, that the upward swimming speed V(up) proportional to N (0.28) and the total swimming force F(S) proportional to N (0.77) (N = colony cell number). These allometric relationships have been important supporting evidence for reaching the conclusion that as size increases, colonies have to invest in cell specialization and increase their S/R to increase their motility capabilities to stay afloat and motile.
• MICHOD, R. (2005). ON FITNESS AND ADAPTEDNESS AND THEIR ROLE IN EVOLUTIONARY EXPLANATION. JOURNAL OF THE HISTORY OF BIOLOGY, 19(2), 289-302.
• Michod, R. (2005). What good is sex?. SCIENCES-NEW YORK, 37(5), 42-46.
• Michod, R. E. (2005). John Maynard Smith.. Annual review of genetics., 39, 1-8.
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  PMID: 16285849;Abstract: John Maynard Smith was one of the most original thinkers in evolutionary biology of the post neo-Darwinian synthesis age. He was able to define new problems with clarity and by doing so open up new research directions. He did this in a number of areas including game theory and evolution, the evolution of sex, animal behavior, evolutionary transitions and molecular evolution. Although he is best known for his research and his ideas, he was a great expositor and wrote many books, including introductory texts in the areas of evolution and genetics, ecology and mathematical modeling, as well as advanced expositions of research problems.
• Michod, R. E. (2005). On the transfer of fitness from the cell to the multicellular organism. Biology and Philosophy, 20(5), 967-987.
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  Abstract: The fitness of any evolutionary unit can be understood in terms of its two basic components: Fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ-soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae - which contain both unicellular and multicellular members - to illustrate the principles and conclusions discussed. © Springer 2005.
• Michod, R. (2004). On the transfer of fitness from the cell to the multicellular organism. BIOLOGY & PHILOSOPHY, 20(5), 967-987.
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  The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ-soma specialization and the emergence of individuality tit the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group Size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae - which contain both unicellular and multicellular members - to illustrate the principles and conclusions discussed.
• Nedelcu, A. M., Marcu, O., & Michod, R. E. (2004). Sex as a response to oxidative stress: A twofold increase in cellular reactive oxygen species activates sex genes. Proceedings of the Royal Society B: Biological Sciences, 271(1548), 1591-1596.
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  PMID: 15306305;PMCID: PMC1691771;Abstract: Organisms are constantly subjected to factors that can alter the cellular redox balance and result in the formation of a series of highly reactive molecules known as reactive oxygen species (ROS). As ROS can be damaging to biological structures, cells evolved a series of mechanisms (e.g. cell-cycle arrest, programmed cell death) to respond to high levels of ROS (i.e. oxidative stress). Recently, we presented evidence that in a facultatively sexual lineage - the multicellular green alga Volvox carteri - sex is an additional response to increased levels of stress, and probably ROS and DNA damage. Here we show that, in V. carteri, (i) sex is triggered by an approximately twofold increase in the level of cellular ROS (induced either by the natural sex-inducing stress, namely heat, or by blocking the mitochondrial electron transport chain with antimycin A), and (ii) ROS are responsible for the activation of sex genes. As most types of stress result in the overproduction of ROS, we believe that our findings will prove to extend to other facultatively sexual lineages, which could be indicative of the ancestral role of sex as an adaptive response to stress and ROS-induced DNA damage.
• ANDERSON, W., AYALA, F., & MICHOD, R. (2003). CHROMOSOMAL AND ALLOZYMIC DIAGNOSIS OF 3 SPECIES OF DROSOPHILA - DROSOPHILA-PSEUDOOBSCURA, DROSOPHILA-PERSIMILIS, AND DROSOPHILA-MIRANDA. JOURNAL OF HEREDITY, 68(2), 71-74.
• MICHOD, R. (2003). EVOLUTION OF INTERACTIONS IN FAMILY-STRUCTURED POPULATIONS - MIXED MATING MODELS. GENETICS, 96(1), 275-296.
• Michod, R. E., & Nedelcu, A. M. (2003). On the reorganization of fitness during evolutionary transitions in individuality. Integrative and Comparative Biology, 43(1), 64-73.
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  PMID: 21680410;Abstract: The basic problem in an evolutionary transition is to understand how a group of individuals becomes a new kind of individual, possessing the property of heritable variation in fitness at the new level of organization. During an evolutionary transition, for example, from single cells to multicellular organisms, the new higher-level evolutionary unit (multicellular organism) gains its emergent properties by virtue of the interactions among lower-level units (cells). We see the formation of cooperative interactions among lower-level units as a necessary step in evolutionary transitions; only cooperation transfers fitness from lower levels (costs to group members) to higher levels (benefits to the group). As cooperation creates new levels of fitness, it creates the opportunity for conflict between levels as deleterious mutants arise and spread within the group. Fundamental to the emergence of a new higher-level unit is the mediation of conflict among lower-level units in favor of the higher-level unit. The acquisition of heritable variation in fitness at the new level, via conflict mediation, requires the reorganization of the basic components of fitness (survival and reproduction) and life-properties (such as immortality and totipotency) as well as the co-option of lower-level processes for new functions at the higher level. The way in which the conflicts associated with the transition in individuality have been mediated, and fitness and general life-traits have been re-organized, can influence the potential for further evolution (i.e., evolvability) of the newly emerged evolutionary individual. We use the volvocalean green algal group as a model-system to understand evolutionary transitions in individuality and to apply and test the theoretical principles presented above. Lastly, we discuss how the different notions of individuality stem from the basic properties of fitness in a multilevel selection context.
• Michod, R. E., Nedelcu, A. M., & Roze, D. (2003). Cooperation and conflict in the evolution of individuality: IV. Conflict mediation and evolvability in Volvox carteri. BioSystems, 69(2-3), 95-114.
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  PMID: 12689724;Abstract: The continued well being of evolutionary individuals (units of selection and evolution) depends upon their evolvability, that is their capacity to generate and evolve adaptations at their level of organization, as well as their longer term capacity for diversifying into more complex evolutionary forms. During a transition from a lower- to higher-level individual, such as the transition between unicellular and multicellular organisms, the evolvability of the lower-level (cells) must be restricted, while the evolvability of the new higher-level unit (multicellular organism) must be enhanced. For these reasons, understanding the factors leading to an evolutionary transition should help us to understand the factors underlying the emergence of evolvability of a new evolutionary unit. Cooperation among lower-level units is fundamental to the origin of new functions in the higher-level unit. Cooperation can produce a new more complex evolutionary unit, with the requisite properties of heritable fitness variations, because cooperation trades fitness from a lower-level (the costs of cooperation) to the higher-level (the benefits for the group). For this reason, the evolution of cooperative interactions helps us to understand the origin of new and higher-levels of fitness and organization. As cooperation creates a new level of fitness, it also creates the opportunity for conflict between levels of selection, as deleterious mutants with differing effects at the two levels arise and spread. This conflict can interfere with the evolvability of the higher-level unit, since the lower and higher-levels of selection will often "disagree" on what adaptations are most beneficial to their respective interests. Mediation of this conflict is essential to the emergence of the new evolutionary unit and to its continued evolvability. As an example, we consider the transition from unicellular to multicellular organisms and study the evolution of an early-sequestered germ-line in terms of its role in mediating conflict between the two levels of selection, the cell and the cell group. We apply our theoretical framework to the evolution of germ/soma differentiation in the green algal group Volvocales. In the most complex member of the group, Volvox carteri, the potential conflicts among lower-level cells as to the "right" to reproduce the higher-level individual (i.e. the colony) have been mediated by restricting immortality and totipotency to the germ-line. However, this mediation, and the evolution of an early segregated germ-line, was achieved by suppressing mitotic and differentiation capabilities in all post-embryonic cells. By handicapping the soma in this way, individuality is ensured, but the solution has affected the long-term evolvability of this lineage. We think that although conflict mediation is pivotal to the emergence of individuality at the higher-level, the way in which the mediation is achieved can greatly affect the longer-term evolvability of the lineage. © 2002 Elsevier Science Ireland Ltd. All rights reserved.
• Nedelcu, A. M., & Michod, R. E. (2003). Sex as a response to oxidative stress: The effect of antioxidants on sexual induction in a facultatively sexual lineage. Proceedings of the Royal Society B: Biological Sciences, 270(SUPPL. 2), s136-s139.
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  PMID: 14667362;PMCID: PMC1809951;Abstract: The evolution of sex is one of the long-standing unsolved problems in biology. Although in many lineages sex is an obligatory part of the life cycle and is associated with reproduction, in prokaryotes and many lower eukaryotes, sex is facultative, occurs in response to stress and often involves the formation of a stress-resistant dormant form. The proximate and ultimate causes of the connection between stress and sex in facultatively sexual lineages are unclear. Because most forms of stress result in the overproduction of cellular reactive oxygen species (ROS), we address the hypothesis that this connection involves ROS and possibly reflects the ancestral role of sex as an adaptive response to the damaging effects of stress-induced ROS (i.e. oxidative stress). Here, we report that two antioxidants inhibit sexual induction in a facultatively sexual species - the multicellular green alga, Volvox carteri. Furthermore, the nature of the sex response and the effect of an iron chelator on sexual induction are consistent with sex being a response to the DNA-damaging effects of ROS. In addition, we present preliminary data to suggest that sex, cell-cycle arrest and apoptosis are alternative responses to increased levels of oxidative stress.
• MICHOD, R. (2001). GENETIC ERROR, SEX, AND DIPLOIDY. JOURNAL OF HEREDITY, 84(5), 360-371.
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  Mathematical models and experiments on transformation are reported testing the hypothesis that sex and diploidy evolved as a DNA repair system. The models focus on the origin of diploidy and sex by studying selection between asexual haploids, sexual haploids, and diploids. Haploid cells are efficient replicators, while diploid cells are resistance to damage. A sexual haploid may combine the advantages of both: spending much of its life cycle in the haploid state, then temporarily fusing to become diploid, followed by splitting to the haploid state. During the diploid state DNA damage can be repaired, since there are two copies of the gene in the cell and one copy is presumed to be undamaged. Five basic rate parameters are employed: birth and death; genomic damage (for the haploids alone); and, for the sexual cell, fusion and splitting. Parameter space bifurcation diagrams for the equilibria are drawn, and solutions of the equations are described in terms of these diagrams. Each type of cell has a region of the parameter space that it occupies exclusively (given its initial presence in the competition). The haploid wins in environments characterized by low damage. The diploid wins in environments characterized by high damage, low mortality, and abundant resources. In general, only a single type of cell occupies a given portion of the space. We find, however, that competitive coexistence of an asexual diploid and sexual haploid is possible in spite of the fact that they are competing for a single resource (nucleotide building blocks). Sex can increase from rarity if matings occur with asexual cells. Only sex can cope with both high mortality and high damage. We then turn to natural bacterial transformation as a model system for the experimental study of sex. Natural transformation in distributed widely, but apparently sparsely, in all bacterial groups. A very preliminary phylogenetic analysis of the bacilli and related species indicates that transformation is probably not a diversifying force in bacterial evolution. However, it is difficult to be sure because of the ambiguity surrounding negative data. Experiments with the bacterium Bacillus subtilis indicate that transformation frequencies respond adaptively to DNA damage if homologous donor DNA is used. Several specific hypotheses for this response are considered. Recent work in other labs on the evolution of transformation is discussed from the point of view of the hypothesis that transformation functions in DNA repair.
• Michod, R. E., & Roze, D. (2001). Cooperation and conflict in the evolution of multicellularity. Heredity, 86(1), 1-7.
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  PMID: 11298810;Abstract: Multicellular organisms probably originated as groups of cells formed in several ways, including cell proliferation from a group of founder cells and aggregation. Cooperation among cells benefits the group, but may be costly (altruistic) or beneficial (synergistic) to individual cooperating cells. In this paper, we study conflict mediation, the process by which genetic modifiers evolve that enhance cooperation by altering the parameters of development or rules of formation of cell groups. We are particularly interested in the conditions under which these modifiers lead to a new higher-level unit of selection with increased cooperation among group members and heritable variation in fitness at the group level. By sculpting the fitness variation and opportunity for selection at the two levels, conflict modifiers create new functions at the organism level. An organism is more than a group of cooperating cells related by common descent; organisms require adaptations that regulate conflict within. Otherwise their continued evolution is frustrated by the creation of within-organism variation and conflict between levels of selection. The evolution of conflict modifiers is a necessary prerequisite to the emergence of individuality and the continued well being of the organism. Conflict leads - through the evolution of adaptations that reduce it - to greater individuality and harmony for the organism.
• Roze, D., & Michod, R. E. (2001). Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity. American Naturalist, 158(6), 638-654.
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  PMID: 18707357;Abstract: Evolutionary transitions require the organization of genetic variation at two (or more) levels of selection so that fitness heritability may emerge at the new level. In this article, we consider the consequences for fitness variation and heritability of two of the main modes of reproduction used in multicellular organisms: vegetative reproduction and single-cell reproduction. We study a model where simple cell colonies reproduce by fragments or propagules of differing size, with mutations occurring during colony growth. Mutations are deleterious at the colony level but can be advantageous or deleterious at the cell level ("selfish" or "uniformly deleterious" mutants). Fragment size affects fitness in two ways: through a direct effect on adult group size (which in turn affects fitness) and by affecting the within- and between-group variances and opportunity for selection on mutations at the two levels. We show that the evolution of fragment size is determined primarily by its direct effects on group size except when mutations are selfish. When mutations are selfish, smaller propagule size may be selected, including single-cell reproduction, even though smaller propagule size has a direct fitness cost by virtue of producing smaller organisms, that is, smaller adult cell groups.
• Roze, D., & Michod, R. E. (2001). Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity. The American naturalist, 158(6), 638-54.
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  Evolutionary transitions require the organization of genetic variation at two (or more) levels of selection so that fitness heritability may emerge at the new level. In this article, we consider the consequences for fitness variation and heritability of two of the main modes of reproduction used in multicellular organisms: vegetative reproduction and single-cell reproduction. We study a model where simple cell colonies reproduce by fragments or propagules of differing size, with mutations occurring during colony growth. Mutations are deleterious at the colony level but can be advantageous or deleterious at the cell level ("selfish" or "uniformly deleterious" mutants). Fragment size affects fitness in two ways: through a direct effect on adult group size (which in turn affects fitness) and by affecting the within- and between-group variances and opportunity for selection on mutations at the two levels. We show that the evolution of fragment size is determined primarily by its direct effects on group size except when mutations are selfish. When mutations are selfish, smaller propagule size may be selected, including single-cell reproduction, even though smaller propagule size has a direct fitness cost by virtue of producing smaller organisms, that is, smaller adult cell groups.
• TORO, M., ABUGOV, R., CHARLESWORTH, B., & MICHOD, R. (2001). EXACT VERSUS HEURISTIC MODELS OF KIN SELECTION. JOURNAL OF THEORETICAL BIOLOGY, 97(4), 699-713.
• WOJCIECHOWSKI, M., HOELZER, M., & MICHOD, R. (2001). DNA-REPAIR AND THE EVOLUTION OF TRANSFORMATION IN BACILLUS-SUBTILIS .2. ROLE OF INDUCIBLE REPAIR. GENETICS, 121(3), 411-422.
• MICHOD, R. (1998). EVOLUTION OF LIFE HISTORIES IN RESPONSE TO AGE-SPECIFIC MORTALITY FACTORS. AMERICAN NATURALIST, 113(4), 531-550.
• MICHOD, R., & WOJCIECHOWSKI, M. (1998). DNA-REPAIR AND THE EVOLUTION OF TRANSFORMATION .4. DNA-DAMAGE INCREASES TRANSFORMATION. JOURNAL OF EVOLUTIONARY BIOLOGY, 7(2), 147-175.
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  Natural genetic transformation in the bacterium Bacillus subtilis provides a model system to explore the evolutionary function of sexual recombination. In the present work, we study the response of transformation to UV irradiation using donor DNAs that differ in sequence homology to the recipient's chromosome and in the mechanism of transformation. The four donor DNAs used include homologous-chromosomal-DNA, two plasmids containing a fragment of B. subtilis trp+ operon DNA and a plasmid with no sequence homology to the recipient cell's DNA. Transformation frequencies for these DNA molecules increase with increasing levels of DNA damage (UV radiation) to recipient cells, only if their transformation requires homologous recombination (i.e. is recA+-dependent). Transformation with non-homologous DNA is independent of the recipient's recombination system and transformation frequencies for it do not respond to increases in UV radiation. The transformation frequency for a selectable marker increases in response to DNA damage more dramatically when the locus is present on small, plasmid-borne, homologous fragments than if it is carried on high molecular weight chromosomal fragments. We also study the kinetics of transformation for the different donor DNAs. Different kinetics are observed for homologous transformation depending on whether the homologous locus is carried on a plasmid or on chromosomal fragments. Chromosomal DNA- and non-homologous-plasmid-DNA-mediated transformation is complete (maximal) within several minutes, while transformation with a plasmid containing homologous DNA is still occurring after an hour. The results indicate that DNA damage directly increases rates of homologous recombination and transformation in B. subtilis. The relevance of these results and recent results of other labs to the evolution of transformation are discussed.
• Michod, R. E. (1998). Origin of sex for error repair: III. Selfish sex. Theoretical Population Biology, 53(1), 60-74.
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  PMID: 9500911;Abstract: According to the repair hypothesis, sex originated as a cooperative interaction-the benefit being damage repair. As with all cooperative strategies, cooperative sex may be vulnerable to selfish mutants. The purpose of the present paper is to understand what implications such selfish mutants may have both for the origin of sex, especially in competition with asexual diploidy, and for the elaboration of the sexual cycle, especially in facultatively sexual organisms. Asexual diploids are assumed to effectively and instantaneously repair all damages without expression of deleterious recessive mutations. Costs to asexual diploidy are considered in terms of its birth rate and mortality rate. The main results of the present paper are as follows. (i) Asexual diploidy wins when the costs of diploidy are small, mortality rates low, and damage rates high. (ii) Beginning with an ancestral state in which cells are asexual haploids, the sexual life cycle would emerge before asexual diploidy as a response to increasing DNA damage. (iii) Selfish sex is a far more robust repair strategy than cooperative sex, especially in competition with asexual diploidy. (iv) Although cooperative sex is more adaptive in extreme environments characterized by high damage and high mortality, selfish sex can still invade in these regions and take the entire system to extinction. (v) Once it is present, selfish sex is stable to asexual diploidy over a wide range of parameter values and can persist in regions of parameter space forbidded to the asexual diploid. These results help to address a concern of the gene repair theory of sex, which is that efficient repair in an asexual diploid is a better strategy than sex. Data from microbes bearing on the results are discussed as is the relationship between facultative sex in multicellular organisms and selfish sex in microbes.
• Nedelcu, A., & Michod, R. (1998). Sex as a response to oxidative stress: the effect of antioxidants on sexual induction in a facultatively sexual lineage. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 270, S136-S139.
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  The evolution of sex is one of the long-standing unsolved problems in biology. Although in many lineages sex is an obligatory part of the life cycle and is associated with reproduction, in prokaryotes and many lower eukaryotes, sex is facultative, occurs in response to stress and often involves the formation of a stress-resistant dormant form. The proximate and ultimate causes of the connection between stress and sex in facultatively sexual lineages are unclear. Because most forms of stress result in the overproduction of cellular reactive oxygen species (ROS), we address the hypothesis that this connection involves ROS and possibly reflects the ancestral role of sex as an adaptive response to the damaging effects of stress-induced ROS (i.e. oxidative stress) . Here, we report that two antioxidants inhibit sexual induction in a facultatively sexual species-the multicellular green alga, Volvox carteri. Furthermore, the nature of the sex response and the effect of an iron chelator on sexual induction are consistent with sex being a response to the DNA-damaging effects of ROS. In addition, we present preliminary data to suggest that sex, cell-cycle arrest and apoptosis are alternative responses to increased levels of oxidative stress.
• Hanschen, E. R., Ferris, P. J., & Michod, R. E. (1997). EARLY EVOLUTION OF THE GENETIC BASIS FOR SOMA IN THE VOLVOCACEAE. EVOLUTION, 68(7), 2014-2025.
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  To understand the hierarchy of life in evolutionary terms, we must explain why groups of one kind of individual, say cells, evolve into a new higher level individual, a multicellular organism. A fundamental step in this process is the division of labor into nonreproductive altruistic soma. The regA gene is critical for somatic differentiation in Volvox carteri, a multicellular species of volvocine algae. We report the sequence of regA-like genes and several syntenic markers from divergent species of Volvox. We show that regA evolved early in the volvocines and predict that lineages with and without soma descended from a regA-containing ancestor. We hypothesize an alternate evolutionary history of regA than the prevailing "proto-regA" hypothesis. The variation in presence of soma may be explained by multiple lineages independently evolving soma utilizing regA or alternate genetic pathways. Our prediction that the genetic basis for soma exists in species without somatic cells raises a number of questions, most fundamentally, under what conditions would species with the genetic potential for soma, and hence greater individuality, not evolve these traits. We conclude that the evolution of individuality in the volvocine algae is more complicated and labile than previously appreciated on theoretical grounds.
• Michod, R. E. (1997). Cooperation and conflict in the evolution of individuality. I. Multilevel selection of the organism. American Naturalist, 149(4), 607-645.
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  Abstract: This article studies the transition in evolution from cells to multicellular organisms. The issues considered are applicable to all major transitions in the units of evolution that share two themes: the emergence of cooperation and the regulation of conflict among the lower-level units, in this case, cells. Explicit genetic models of mutation and selection both within and between organisms are studied in sexual and asexual haploid and diploid organisms without a germ line. The results may be understood in terms of the differing opportunities for within-and between-organism selection under the different reproductive modes and parameter values. Cooperation among cells increases when the fitness covariance at the level of the organism overcomes within-organism change toward defecting cells. Selection and mutation during development generate significant levels of within-organism variation and lead to significant variation in organism fitness at equilibrium. The levels of cooperativity attained can be low, even with reproduction passing through a single-cell zygote stage and the high kinship that entails. Sex serves to maintain higher levels of cooperation and lower levels of within-organism change. Fixed size may help organisms reduce conflict among cells.
• Michod, R. E. (1997). Evolution of individuality during the transition from unicellular to multicellular life. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 104, 8613-8618.
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  Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.
• Michod, R. E. (1997). Evolution of the individual. American Naturalist, 150(SUPPL.), S5-S21.
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  PMID: 18811312;Abstract: This article studies the transitions in evolution from single cells to multicellular organisms as a case study in the origin of individuality. TIle issues considered are applicable to all major transitions in the units of selection that involve the emergence of cooperation and the regulation of conflict. Explicit genetic models of mutation and selection both within and between organisms are studied. Cooperation among cells increases when the fitness covariance at the level el the organism overcomes within-organism change toward defection. Selection and mutation during development generate significant levels of within-organism variation and lead to variation in organism fitness at equilibrium. This variation selects for germ-line modifiers and other mediators of within-organism conflict, increasing the heritability of fitness at the organism level. The evolution of those modifiers is the first new function at the emerging organism level a necessary component of the evolution of individuality.
• Michod, R. E. (1997). The group covariance effect and fitness trade-offs during evolutionary transitions in individuality. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 103(24), 9113-9117.
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  Transforming our understanding of life is the realization that evolution occurs not only among individuals within populations but also through the integration of groups of preexisting individuals into a new higher-level individual, that is, through evolutionary transitions in individuality. During evolutionary transitions (such as during the origin of gene networks, bacteria-like cells, eukaryotic cells, multicellular organisms, and societies), fitness must be reorganized; specifically, it must be transferred from the lower- to the higher-level units and partitioned among the lower-level units that specialize in the fitness components of the new higher-level individual. This paper studies the role of fitness trade-offs in fitness reorganization, the evolution of cooperation, and the conversion of a group into a new individual during the origin of multicellular life. Specifically, this study shows that the fitness of the group is augmented over the average fitness of its members according to a covariance effect. This covariance effect appears to be one of the first emergent properties of the group and a general aspect of groups with multiplicative properties that are themselves averages of properties of lower-level units. The covariance effect allows groups to break through the constraints that govern their members, and this effect likely applies to group dynamics in other fields.
• Michod, R. E., & Roze, D. (1997). Transitions in individuality. Proceedings of the Royal Society B: Biological Sciences, 264(1383), 853-857.
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  PMID: 9225477;PMCID: PMC1688438;Abstract: The evolution of multicellular organisms is the premier example of the integration of lower levels into a single, higher-level individual. Explaining the evolutionary transition from single cells to multicellular organisms is a major challenge for evolutionary theory. We provide an explicit framework for understanding this transition in terms of the increase of cooperation among cells and the regulation of conflict within the emerging organism. Heritability of fitness and individuality at the new level emerge as a result of the evolution of organismal functions that restrict the opportunity for conflict within and ensure cooperation among cells. Conflict leads, through the evolution of adaptations that reduce it, to greater individuality and harmony for the organism.
• Shelton, D. E., Desnitskiy, A. G., & Michod, R. E. (1997). Distributions of reproductive and somatic cell numbers in diverse Volvox (Chlorophyta) species. EVOLUTIONARY ECOLOGY RESEARCH, 14(6), 707-727.
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  Background: Volvox (Chlorophyta) asexual colonies consist of two kinds of cells: a large number of small somatic cells and a few large reproductive cells. The numbers of reproductive and somatic cells correspond directly to the major components of fitness fecundity and viability, respectively. Volvox species display diverse patterns of development that give rise to the two cell types.
• Ferriere, R., & Michod, R. E. (1996). The evolution of cooperation in spatially heterogeneous populations. American Naturalist, 147(5), 692-717.
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  Abstract: A challenging problem in sociobiology is to understand the emergence of cooperation in a nonsocial world. Recent models of the iterated Prisoner's Dilemma (IPD) game conclude that population mixing due to individual mobility limits cooperation; however, these models represent space only implicitly. Here we develop a dynamical IPD model where temporal and spatial variations in the population are explicitly considered. Our model accounts for the stochastic motion of individuals and the inherent nonrandomness of local interactions. By deriving a spatial version of Hamilton's rule, we find that a threshold level of mobility in selfish always-defect (AD) players is required to beget invasion by social "tit for tat" (TFT) players. Furthermore, the level of mobility of successful TFT newcomers must be approximately equal to or somewhat higher than that of resident defectors. Significant mobility promotes the assortment of TFT pioneers on the front of invasion and of AD intruders in the core of a cooperative cluster. It also maximizes the likelihood of TFT retaliation. Once this first step whereby TFT takes over AD is completed, more generous and perhaps more suspicious strategies may outperform and displace TFT. We derive the conditions under which this continued evolution of more robust cooperative strategies occurs.
• Herron, M. D., Desnitskiy, A. G., & Michod, R. E. (1996). EVOLUTION OF DEVELOPMENTAL PROGRAMS IN VOLVOX (CHLOROPHYTA). JOURNAL OF PHYCOLOGY, 46(2), 316-324.
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  The volvocine green algal genus Volvox includes similar to 20 species with diverse sizes (in terms of both diameter and cell number), morphologies, and developmental programs. Two suites of characters are shared among distantly related lineages within Volvox. The traits characteristic of all species of Volvox-large (> 500) numbers of small somatic cells, much smaller numbers of reproductive cells, and oogamy in sexual reproduction-have three or possibly four separate origins. In addition, some species have evolved a suite of developmental characters that differs from the ancestral developmental program. Most multicellular volvocine algae, including some species of Volvox, share an unusual pattern of cell division known as palintomy or multiple fission. Asexual reproductive cells (gonidia) grow up to many times their initial size and then divide several times in rapid succession, with little or no growth between divisions. Three separate Volvox lineages have evolved a reduced form of palintomy in which reproductive cells are small and grow between cell divisions. In each case, these changes are accompanied by a reduction in the rate of cell division and by a requirement of light for cell division to occur. Thus, two suites of characters-those characteristic of all Volvox species and those related to reduced palintomy-have each evolved convergently or in parallel in lineages that diverged at least 175 million years ago (mya).
• Michod, R. E. (1996). Cooperation and conflict in the evolution of individuality. II. Conflict mediation. Proceedings of the Royal Society B: Biological Sciences, 263(1372), 813-822.
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  PMID: 8760489;Abstract: Evolutionary transitions in the units of selection require the promotion of cooperation and the regulation of conflict among the lower level units. For multicellular organisms to emerge as a new unit of selection, the selfish tendencies of their component cells had to be controlled. Theoretical results indicate organisms may regulate this internal conflict and competition in several ways: by reducing the somatic mutation rate, by sequestering cells in a germ line and by directly reducing the benefits to cells of defecting.
• FERRIERE, R., & MICHOD, R. (1995). INVADING WAVE OF COOPERATION IN A SPATIAL ITERATED PRISONERS-DILEMMA. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 259(1354), 77-83.
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  Explaining the emergence of cooperative behaviours in a selfish world remains a major challenge for sociobiology. The iterated prisoner's dilemma offers a well-studied metaphor with which to explore theoretically the evolution of cooperation by reciprocation. Our current understanding is that 'tit-for-tat' should be the very first step (if not the aim) of evolution towards cooperation, but that mobility of the players in space seems to raise a devastating obstacle to the spread of tit-for-tat, by allowing egoists to exploit cooperation and escape retaliation. The second point is based on models that represent mobility only implicitly (in terms of travelling costs) and assume random interactions. Here we develop a more explicit theory of spatial iterated games: individual mobility is represented in terms of a diffusion process and interactions - defined locally - are inherently non-random. Our model reveals the existence of critical levels of individual mobility allowing for the evolution of cooperation. In fact, tit-for-tat can spread and take over among mobile players even when originating from extreme rarity. The dynamics of invasion of tit-for-tat develop as a travelling wave which propagates the cooperative strategy through space. Significant mobility is required to make the pioneering moves of cooperators towards the front of invasion less hazardous; it also contributes to neutralizing those defectors who may intrude the core of a cluster of cooperative players.
• Ferriere, R., & Michod, R. E. (1995). Invading wave of cooperation in a spatial iterated prisoner's dilemma. Proceedings of the Royal Society B: Biological Sciences, 259(1354), 77-83.
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  PMID: 7700879;Abstract: Explaining the emergence of cooperative behaviours in a selfish world remains a major challenge for sociobiology. The iterated prisoner's dilemma offers a well-studied metaphor with which to explore theoretically the evolution of cooperation by reciprocation. Our current understanding is that 'tit-for-tat' should be the very first step (if not the aim) of evolution towards cooperation, but that mobility of the players in space seems to raise a devastating obstacle to the spread of tit-for-tat, by allowing egoists to exploit cooperation and escape retaliation. The second point is based on models that represent mobility only implicitly (in terms of travelling costs) and assume random interactions. Here we develop a more explicit theory of spatial iterated games: individual mobility is represented in terms of a diffusion process and interactions - defined locally - are inherently non-random. Our model reveals the existence of critical levels of individual mobility allowing for the evolution of cooperation. In fact, tit-for-tat can spread and take over among mobile players even when originating from extreme rarity. The dynamics of invasion of tit-for-tat develop as a travelling wave which propagates the cooperative strategy through space. Significant mobility is required to make the pioneering moves of cooperators towards the front of invasion less hazardous; it also contributes to neutralizing those defectors who may intrude the core of a cluster of cooperative players.
• Long, A., & Michod, R. E. (1995). Origin of sex for error repair. 1. Sex, diploidy, and haploidy. Theoretical Population Biology, 47(1), 18-55.
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  PMID: 7709368;
• Michod, R. E., & Long, A. (1995). Origin of sex for error repair. 2. Rarity and extreme environments. Theoretical Population Biology, 47(1), 56-81.
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  PMID: 7709369;
• Smith, D. R., Hamaji, T., Olson, B. J., Durand, P. M., Ferris, P., Michod, R. E., Featherston, J., Nozaki, H., & Keeling, P. J. (1995). Organelle Genome Complexity Scales Positively with Organism Size in Volvocine Green Algae. MOLECULAR BIOLOGY AND EVOLUTION, 30(4), 793-797.
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  It has been argued that for certain lineages, noncoding DNA expansion is a consequence of the increased random genetic drift associated with long-term escalations in organism size. But a lack of data has prevented the investigation of this hypothesis in most plastid-bearing protists. Here, using newly sequenced mitochondrial and plastid genomes, we explore the relationship between organelle DNA noncoding content and organism size within volvocine green algae. By looking at unicellular, colonial, and differentiated multicellular algae, we show that organelle DNA complexity scales positively with species size and cell number across the volvocine lineage. Moreover, silent-site genetic diversity data suggest that the volvocine species with the largest cell numbers and most bloated organelle genomes have the smallest effective population sizes. Together, these findings support the view that nonadaptive processes, like random genetic drift, promote the expansion of noncoding regions in organelle genomes.
• Michod, R. (1994). Origin of sex for error repair - III. Selfish sex. THEORETICAL POPULATION BIOLOGY, 53(1), 60-74.
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  According to the repair hypothesis, sex originated as a cooperative interaction-the benefit being damage repair, As with all cooperative strategies, cooperative sex may be vulnerable to selfish mutants, The purpose of the present paper is to understand what implications such selfish mutants may have both for the origin of sex, especially in competition with asexual diploidy, and for the elaboration of the sexual cycle, expecially in facultatively sexual organisms, Asexual diploids are assumed to effectively and instantaneously repair all damages without expression of deleterious recessive mutations. Costs to asexual diploidy are considered in terms of its birth rate and mortality rate, The main results of the present paper are as follows. (i) Asexual diploidy wins when the costs of diploidy are small, mortality rates low, and damage Fates high. (ii) Beginning with an ancestral state in which cells are asexual haploids, the sexual life cycle would emerge before asexual diploidy as a response to increasing DNA damage. (iii) Selfish sex is a far more robust repair strategy than cooperative sex, especially in competition with asexual diploidy. (iv) Although cooperative sex is more adaptive in extreme environments characterized by high damage and high mortality, selfish sex can still invade In these regions and take the entire system to extinction. (v) Once it is present, selfish sex is stable to asexual diploidy over a wide range of parameter values and can persist in regions of parameter space forbidded to the asexual diploid. These results help to address a concern of the gene repair theory of sex, which is that efficient: repair in an asexual diploid is a better strategy than sex, Data fram microbes hearing on the results are discussed as is the relationship between facultative sex in multicellular organisms and selfish sex in microbes. (C) 1998 Academic Press.
• Michod, R. E., & Wojciechowski, M. F. (1994). DNA repair and the evolution of transformation IV. DNA damage increases transformation. Journal of Evolutionary Biology, 7(2), 147-175.
• Shelton, D. E., & Michod, R. E. (1994). Philosophical foundations for the hierarchy of life. BIOLOGY & PHILOSOPHY, 25(3), 391-403.
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  We review Evolution and the Levels of Selection by Samir Okasha. This important book provides a cohesive philosophical framework for understanding levels-of-selections problems in biology. Concerning evolutionary transitions, Okasha proposes that three stages characterize the shift from a lower level of selection to a higher one. We discuss the application of Okasha's three-stage concept to the evolutionary transition from unicellularity to multicellularity in the volvocine green algae. Okasha's concepts are a provocative step towards a more general understanding of the major evolutionary transitions; however, the application of certain ideas to the volvocine model system is not straightforward.
• ABUGOV, R., & MICHOD, R. (1993). ON THE RELATION OF FAMILY STRUCTURED MODELS AND INCLUSIVE FITNESS MODELS FOR KIN SELECTION. JOURNAL OF THEORETICAL BIOLOGY, 88(4), 743-754.
• MICHOD, R., WOJCIECHOWSKI, M., & HOELZER, M. (1993). DNA-REPAIR AND THE EVOLUTION OF TRANSFORMATION IN THE BACTERIUM BACILLUS-SUBTILIS. GENETICS, 118(1), 31-39.
• Michod, R. E. (1993). Genetic error, sex, and diploidy. Journal of Heredity, 84(5), 360-371.
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  PMID: 8409358;
• MICHOD, R., & ABUGOV, R. (1992). ADAPTIVE TOPOGRAPHY IN FAMILY-STRUCTURED MODELS OF KIN SELECTION. SCIENCE, 210(4470), 667-669.
• BYERLY, H., & MICHOD, R. (1991). FITNESS AND EVOLUTIONARY EXPLANATION. BIOLOGY & PHILOSOPHY, 6(1), 1-22.
• Byerly, H. C., & Michod, R. E. (1991). Fitness and evolutionary explanation. Biology & Philosophy, 6(1), 1-22.
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  Abstract: Recent philosophical discussions have failed to clarify the roles of the concept fitness in evolutionary theory. Neither the propensity interpretation of fitness nor the construal of fitness as a primitive theoretical term succeed in explicating the empirical content and explanatory power of the theory of natural selection. By appealing to the structure of simple mathematical models of natural selection, the authors separate different contrasts which have tended to confuse discussions of fitness: the distinction between what fitness is defined as versus what fitness is a function of; the contrast between adaptedness as an overall property of organisms and specific adaptive capacities; the distinction between actual and potential reproductive success; the role of chance vs systematic causal relations; fitness as applied to organisms as opposed to fitness applied to genotype classes; heritable adaptive capacities of genotypes as opposed to relations between genotypes and the environment. (See also 92L/01109) . -from Authors
• Hoelzer, M. A., & Michod, R. E. (1991). DNA repair and the evolution of transformation in Bacillus subtilis. III. Sex with damaged DNA. Genetics, 128(2), 215-223.
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  PMID: 1906416;PMCID: PMC1204460;Abstract: Natural genetic transformation in the bacterium Bacillus subtilis provides an experimental system for studying the evolutionary function of sexual recombination. The repair hypothesis proposes that during transformation the exogenous DNA taken up by cells is used as template for recombinational repair of damages in the recipient cell's genome. Earlier results demonstrated that the population density of transformed cells (i.e., sexual cells) increases, relative to nontransformed cells (primarily asexual cells), with increasing dosage of ultraviolet irradiation, provided that the cells are transformed with undamaged homologous DNA after they have become damaged. In nature, however, donor DNA for transformation is likely to come from cells that are as damaged as the recipient cells. In order to better simulate the effects of transformation in natural populations we conducted similar experiments as those just described using damaged donor DNA. We document in this report that transformants continue to increase in relative density even if they are transformed with damaged donor DNA. These results suggest that sites of transformation are often damaged sites in the recipient cell's genome.
• MICHOD, R., & ANDERSON, W. (1991). ON CALCULATING DEMOGRAPHIC PARAMETERS FROM AGE FREQUENCY DATA. ECOLOGY, 61(2), 265-269.
• Gayley, T. W., & Michod, R. E. (1990). Modification of genetic constraints on frequency-dependent selection. American Naturalist, 136(3), 406-427.
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  Abstract: The prediction of phenotypic equilibrium states through reasoning about evolutionarily stable states (ESS's) is commonplace in evolutionary biology. When there is a specific genetic system underlying the transmission of phenotypes, however, genetic constraints may prevent the realization of phenotypic equilibria. With two-strategy games and a one-locus genetic system, the direction of selection is always toward an ESS, and all stable genetic equilibria that are not ESS's (non-ES equilibria) can be characterized as being as close to the ESS as the genetic system allows, at least locally. Starting from these non-ES equilibria, a series of computer simulations shows that the evolution of modifier genes at a second locus is expected to move the population closer to the ESS, although there are counterexamples. With multiple-strategy games, the genetic constraints are much more complex. It is not generally the case that genetic equilibria are "close' to the ESS in some sense. -Authors
• Michod, R. (1990). Array. Trends in Neurosciences, 13(1), 12-13.
• Michod, R. (1990). Evolution of sex. Trends in Ecology and Evolution, 5(1), 30-.
• Michod, R. E., & Hasson, O. (1990). On the evolution of reliable indicators of fitness. American Naturalist, 135(6), 788-808.
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  Abstract: Studied the evolution of traits that have conflicting effects on 2 components of fitness in a population in which there are prior heritable viability differences. Examples of such traits may include the conspicuous male traits, or displays, that increase a male's mating success but decrease his viability. The authors consider the case of 2 viability classes controlled by a single haploid locus and a 2nd modifier locus, which modifies the expression of the trait in one or both of the viability classes. Variation at the viability-class locus is maintained by a balance between selection and a force, like mutation or migration, that restores the less fit class. As a result of the prior differences in viability and the effects of the trait, overall fitness in each viability class is maximized at different values (optima) of the trait. In the absence of modifiers that can differentially express the trait in the different viability classes, the evolutionarily stable value of the trait is a compromise between the optimum values for the 2 fitness classes. Modifiers that can act independently on the trait in the 2 viability classes allow the trait to take on its optimum values in the 2 viability classes. Since the optimum of the trait for the high-viability class is greater than that for the low-viability class, evolutionary modification should allow such traits to be used as reliable indicators of genetic fitness. -from Authors
• Michod, R., & Roze, D. (1990). Transitions in individuality. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 264(1383), 853-857.
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  The evolution of multicellular organisms is the premier example of the integration of lower levels into a single, higher-level individual. Explaining the evolutionary transition from single cells to multicellular organisms is a major challenge for evolutionary theory. We provide an explicit two locus genetic framework for understanding this transition in terms of the increase of cooperation among cells and the regulation of conflict within the emerging organism. Heritability of fitness and individuality at the new level emerge as a result of the evolution of organismal functions that restrict the opportunity for conflict within and ensure cooperation among cells. Conflict leads, through the evolution of adaptations that reduce it, to greater individuality and harmony for the organism.
• Shelton, D. E., & Michod, R. E. (1990). Levels of selection and the formal Darwinism project. BIOLOGY & PHILOSOPHY, 29(2), 217-224.
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  Understanding good design requires addressing the question of what units undergo natural selection, thereby becoming adapted. There is, therefore, a natural connection between the formal Darwinism project (which aims to connect population genetics with the evolution of design and fitness maximization) and levels of selection issues. We argue that the formal Darwinism project offers contradictory and confusing lines of thinking concerning level(s) of selection. The project favors multicellular organisms over both the lower (cell) and higher (social group) levels as the level of adaptation. Grafen offers four reasons for giving such special status to multicellular organisms: (1) they lack appreciable within-organism cell selection, (2) they have multiple features that appear contrived for the same purpose, (3) they possess a set of phenotypes, and (4) they leave offspring according to their phenotypes. We discuss why these rationales are not compelling and suggest that a more even-handed approach, in which multicellular organisms are not assumed to have special status, would be desirable for a project that aims to make progress on the foundations of evolutionary theory.
• BERNSTEIN, H., BYERLY, H., HOPF, F., & MICHOD, R. (1989). ORIGIN OF SEX. JOURNAL OF THEORETICAL BIOLOGY, 110(3), 323-351.
• MICHOD, R., & LONG, A. (1989). ORIGIN OF SEX FOR ERROR REPAIR .2. RARITY AND EXTREME ENVIRONMENTS. THEORETICAL POPULATION BIOLOGY, 47(1), 56-81.
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  In a previous paper we studied the simultaneous, and at times conflicting, needs of coping with DNA damage, efficient cell replication, and the avoidance of cell mortality. These selective factors operated on sexual and asexual haploid and diploid populations that were reproductively isolated from one another. We concluded, in part, that a sexual type of cell could not expand from extreme rarity in populations dominated by asexual haploid and diploid cells. In the present paper we show that it is relatively easy for a rare sexual mutant to expand in a population dominated by asexual haploid cells if some matings occur between sexual and asexual cell types. We also study the persistence of sex in high mortality, high damage environments, in which neither the asexual diploid nor haploid can survive. The diploid cannot survive because its lower birth rate cannot overcome mortality and the haploid cannot survive because its birth rate cannot overcome gene damage. Sex can persist in these punishing environments by tuning the parameters of the sexual cycle, and the fusion and splitting rates, into a specified region, thereby reaping both benefits of damage repair and efficient replication. (C) 1995 Academic Press, Inc.
• Wojciechowski, M. F., Hoelzer, M. A., & Michod, R. E. (1989). DNA repair and the evolution of transformation in Bacillus subtilis. II. Role of inducible repair.. Genetics, 121(3), 411-422.
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  PMID: 2497048;PMCID: PMC1203629;Abstract: In Bacillus subtilis, DNA repair and recombination are intimately associated with competence, the physiological state in which the bacterium can bind, take up and recombine exogenous DNA. Previously, we have shown that the homologous DNA transformation rate (ratio of transformants to total cells) increases with increasing UV dosage if cells are transformed after exposure to UV radiation (UV-DNA), whereas the transformation rate decreases if cells are transformed before exposure to UV (DNA-UV). In this report, by using different DNA repair-deficient mutants, we show that the greater increase in transformation rate in UV-DNA experiments than in DNA-UV experiments does not depend upon excision repair or inducible SOS-like repair, although certain quantitative aspects of the response do depend upon these repair systems. We also show that there is no increase in the transformation rate in a UV-DNA experiment when repair and recombination proficient cells are transformed with nonhomologous plasmid DNA, although the results in a DNA-UV experiment are essentially unchanged by using plasmid DNA. We have used din operon fusions as a sensitive means of assaying for the expression of genes under the control of the SOS-like regulon in both competent and noncompetent cell subpopulations as a consequence of competence development and our subsequent experimental treatments. Results indicate that the SOS-like system is induced in both competent and noncompetent subpopulations in our treatments and so should not be a major factor in the differential response in transformation rate observed in UV-DNA and DNA-UV treatments. These results provide further support to the hypothesis that the evolutionary function of competence is to bring DNA into the cell for use as template in the repair of DNA damage.
• BERNSTEIN, H., BYERS, G., & MICHOD, R. (1988). EVOLUTION OF SEXUAL REPRODUCTION - IMPORTANCE OF DNA-REPAIR, COMPLEMENTATION, AND VARIATION. AMERICAN NATURALIST, 117(4), 537-549.
• Durand, P. M., Choudhury, R., Rashidi, A., & Michod, R. E. (1988). Programmed death in a unicellular organism has species-specific fitness effects. BIOLOGY LETTERS, 10(2).
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  Programmed cell death (PCD) is an ancient phenomenon and its origin and maintenance in unicellular life is unclear. We report that programmed death provides differential fitness effects that are species specific in the model organism Chlamydomonas reinhardtii. Remarkably, PCD in this organism not only benefits others of the same species, but also has an inhibitory effect on the growth of other species. These data reveal that the fitness effects of PCD can depend upon genetic relatedness.
• Hopf, F. A., Michod, R. E., & Sanderson, M. J. (1988). The effect of the reproductive system on mutation load. Theoretical Population Biology, 33(3), 243-265.
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  PMID: 3232115;Abstract: J. B. S. Haldane (Amer. Nat. 71, 337-349, 1937) argued that, in equilibrium populations, the effect of deleterious mutation on average fitness depends primarily on the mutation rate and is independent of the severity of the mutations. Specifically, the equilibrium population fitness is e-μH, where μH is the haploid genomic mutation rate. Here we extend Haldane's result to a variety of reproductive systems. Using an analysis based on the frequency of classes of individuals with a specified number of mutations, we show that Haldane's principle holds exactly for haploid sex, haploid apomixis, and facultative haploid sex. In the cases of diploid automixis with terminal fusion, diploid automixis with central fusion, and diploid selfing, Haldane's principle holds exactly for recessive mutations and approximately for mutations with some heterozygous effect. In the cases of K-ploid apomixis, diploid endomitosis, and haplodiploidy, we show that Haldane's principle holds exactly for recessive lethal mutations. In addition we extend Haldane's result to various mixtures of the above-mentioned reproductive systems. In the case of diploid out-crossing sexuals, we do not obtain an exact analytic result, but present arguments and computer simulations which show that Haldane's result extends to this case as well in the limit as the number of loci becomes large. Although diverse reproductive systems are equally fit at equilibrium, different reproductive systems harbor vastly different numbers of recessive genes at equilibrium and we provide estimates of these numbers. These different numbers of mutations may create transient selective pressures on individuals with reproductive systems different from that of the equilibrium population. © 1988.
• Michod, R. E., Wojciechowski, M. F., & Hoezler, M. A. (1988). DNA repair and the evolution of transformation in the bacterium Bacillus subtilis. Genetics, 118(1), 31-39.
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  PMID: 8608929;PMCID: PMC1203263;Abstract: The purpose of the work reported here is to test the hypothesis that natural genetic transformation in the bacterium Bacillus subtilis has evolved as a DNA repair system. Specifically, tests were made to determine whether transformation functions to provide DNA template for the bacterial cell to use in recombinational repair. The survivorship and the homologous transformation rate as a function of dose of ultraviolet irradiation (UV) was studied in two experimental treatments, in which cells were either transformed before (DNA-UV), or after (UV-DNA), treatment with UV. The results show that there is a qualitative difference in the relationship between the survival of transformed cells (sexual cells) and total cells (primarily asexual cells) in the two treatments. As predicted by the repair hypothesis, in the UV-DNA treatment, transformed cells had greater average survivorship than total cells, while in the DNA-UV treatment this relationship was reversed. There was also a consistent and qualitative difference between the UV-DNA and DNA-UV treatments in the relationship between the homologous transformation rate (transformed cells/total cells) and UV dosage. As predicted by the repair hypothesis, the homologous transformation rate increases with UV dose in the UV-DNA experiments but decreases with UV dose in the DNA-UV treatments. However, the transformation rate for plasmid DNA does not increase in a UV-DNA treatment. These results support the DNA repair hypothesis for the evolution of transformation in particular, and sex generally.
• Bernstein, H., Hopf, F. A., & Michod, R. E. (1987). The molecular basis of the evolution of sex.. Advances in genetics, 24, 323-370.
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  PMID: 3324702;Abstract: Traditionally, sexual reproduction has been explained as an adaptation for producing genetic variation through allelic recombination. Serious difficulties with this explanation have led many workers to conclude that the benefit of sex is a major unsolved problem in evolutionary biology. A recent informational approach to this problem has led to the view that the two fundamental aspects of sex, recombination and outcrossing, are adaptive responses to the two major sources of noise in transmitting genetic information, DNA damage and replication errors. We refer to this view as the repair hypothesis, to distinguish it from the traditional variation hypothesis. On the repair hypothesis, recombination is a process for repairing damaged DNA. In dealing with damage, recombination produces a form of informational noise, allelic recombination, as a by-product. Recombinational repair is the only repair process known which can overcome double-strand damages in DNA, and such damages are common in nature. Recombinational repair is prevalent from the simplest to the most complex organisms. It is effective against many different types of DNA-damaging agents, and, in particular, is highly efficient in overcoming double-strand damages. Current understanding of the mechanisms of recombination during meiosis suggests that meiosis is designed for repairing DNA. These considerations form the basis for the first part of the repair hypothesis, that recombination is an adaptation for dealing with DNA damage. The evolution of sex can be viewed as a continuum on the repair hypothesis. Sex is presumed to have arisen in primitive RNA-containing protocells whose sexual process was similar to that of recombinational repair in extent segmented, single-stranded RNA viruses, which are among the simplest known organisms. Although this early form of repair occurred by nonenzymatic reassortment of replicas of undamaged RNA segments, it evolved into enzyme-mediated breakage and exchange between long DNA molecules. As some lines of descent became more complex, their genome information increased, leading to increased vulnerability to mutation. The diploid stage of the sexual cycle, which was at first transient, became the predominant stage in some lines of descent because it allowed complementation, the masking of deleterious recessive mutations. Out-crossing, the second fundamental aspect of sex, is also maintained by the advantage of masking mutations. However, outcrossing can be abandoned in favor of parthenogenesis or selfing under conditions in which the costs of mating are very high.(ABSTRACT TRUNCATED AT 400 WORDS)
• Roze, D., & Michod, R. (1987). Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity. AMERICAN NATURALIST, 158(6), 638-654.
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  Evolutionary transitions require the organization of genetic variation at two (or more) levels of selection so that fitness heritability may emerge at the new level. In this article, we consider the consequences for fitness variation and heritability of two of the main modes of reproduction used in multicellular organisms: vegetative reproduction and single-cell reproduction. We study a model where simple cell colonies reproduce by fragments or propagules of differing size, with mutations occurring during colony growth. Mutations are deleterious at the colony level but can be advantageous or deleterious at the cell level ("selfish" or "uniformly deleterious" mutants). Fragment size affects fitness in two ways: through a direct effect on adult group size (which in turn affects fitness) and by affecting the within- and between-group variances and opportunity for selection on mutations at the two levels. We show that the evolution of fragment size is determined primarily by its direct effects on group size except when mutations are selfish. When mutations are selfish, smaller propagule size may be selected, including single-cell reproduction, even though smaller propagule size has a direct fitness cost by virtue of producing smaller organisms, that is, smaller adult cell groups.
• Michod, R. E. (1986). On fitness and adaptedness and their role in evolutionary explanation. Journal of the History of Biology, 19(2), 289-302.
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  PMID: 11611993;
• BERNSTEIN, H., BYERLY, H., HOPF, F., & MICHOD, R. (1985). GENETIC-DAMAGE, MUTATION, AND THE EVOLUTION OF SEX. SCIENCE, 229(4719), 1277-1281.
• Bernstein, H., Byerly, H. C., Hopf, F. A., & Michod, R. E. (1985). Genetic damage, mutation, and the evolution of sex. Science, 229(4719), 1277-1281.
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  PMID: 3898363;Abstract: The two fundamental aspects of sexual reproduction, recombination and outcrossing, appear to be maintained respectively by the advantages of recombinational repair and genetic complementation. Genetic variation is produced as a by-product of recombinational repair, but it may not be the function of sexual reproduction.
• Bernstein, H., Byerly, H. C., Hopf, F. A., & Michod, R. E. (1985). Sex and the emergence of species. Journal of Theoretical Biology, 117(4), 665-690.
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  PMID: 4094459;Abstract: We argue that the existence of species as distinct and relatively homogeneous groupings of individuals is a consequence of the nonlinear dynamics inherent in sexual reproduction. This approach provides an answer to two interrelated problems which Darwin posed and tried to solve. Why are there missing links (i.e. gaps) between species in habitat space, and why are there missing links between species in time as evidenced in the fossil record? A crucial difference between outcrossing sexual organisms (i.e. organisms in which mating is between different individuals) and obligate selfers or parthenogens lies in the dynamic of the underlying replication process. Replication is a linear function of density for obligate selfers or parthenogens but nonlinear for outcrossing sexuals. The nonlinearity stems from the simple fact that with outcrossing, two individuals must come together to mate. We argue that this fact leads to density dependent fitness (per capita rate of increase) with an intrinsic disadvantage of low population density. This cost of rarity results in a distribution of distinct species. By establishing the causal connections in evolution between outcrossing sex and the very existence of species as distinct collections of organisms, our account lends theoretical support to a unitary concept of species with interbreeding as the fundamental defining property. © 1985 Academic Press Inc. (London) Ltd.
• Bernstein, H., Byerly, H. C., Hopf, F. A., & Michod, R. E. (1985). The evolutionary role of recombinational repair and sex.. International Review of Cytology, 96, 1-28.
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  PMID: 2416705;Abstract: We have argued that sexual reproduction arose very early in the evolution of life as a way of overcoming informational damage or loss through recombinational repair. As organisms became more complex and genome information content expanded, diploidy, at first transient, became the predominant way of coping with increased vulnerability to mutation. This allowed further genome expansion. Once such expansion had occurred, however, diploidy became essentially irreversible, since reversion to haploidy would lead to expression of accumulated deleterious recessive alleles. This expression of recessive alleles also imposes a stiff penalty on organisms that experiment with close inbreeding forms of recombinational repair. A consequence of sex is that fitness (defined as per capita rate of increase) is density dependent. At low population density, fitness declines due to increased costs of finding a mate. This fundamental constraint on population increase can inhibit evolutionary success of the best adapted species if it is small in numbers. Sexual reproduction also tends to eliminate new coadapted genotypes within a species by breaking up their coadapted gene complexes; this also contributes to the cohesion of species. In general, we think the existence of species and their characteristic cohesion and stability over time are direct consequences of sex; and sex in turn is a consequence of the need to overcome gene damage through recombinational repair while at the same time masking the deleterious effects of mutation.
• LONG, A., & MICHOD, R. (1985). ORIGIN OF SEX FOR ERROR REPAIR .1. SEX, DIPLOIDY, AND HAPLOIDY. THEORETICAL POPULATION BIOLOGY, 47(1), 18-55.
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  Genetic damage is a fundamental problem for living systems. Recombination can repair a damaged gene, so long as there is an undamaged copy of the gene available in the cell. This requires that the cell be diploid for the damaged locus. During sex, outcrossing generates the diploid state by temporarily fusing two haploid cells (as in the case of meiosis) or by bringing DNA into the cell from outside (as in the case of bacterial transformation). But why should cells alternate between the haploid and diploid states in the first place? Why not just remain diploid, if damage repair is the only problem for a cell? The goal of our work is to understand if the problem of genetic damage would select for diploidy or for the alternation between diploid and haploid states-that is, sex-early in the history of life. Using mathematical models we study competition between asexual haploids (termed ''haploids''), sexuals (termed ''sexuals''), and asexual diploids (termed ''diploids''). Haploid cells are efficient replicators, while diploid cells are resistant to damage. A sexual may combine the advantages of both: spending much of its life cycle in the haploid state, then temporarily fusing to become diploid, followed by splitting to the haploid state. During the diploid state DNA damage can be repaired, since there are two copies of the gene in the cell and one copy is presumed to be undamaged. We describe the competition in terms of mathematical models, employing five rate parameters which represent the life processes of cells most probably active at the time that sexuality arose: birth and death; genomic damage (for the haploids alone); and, for the sexual cell, fusion and splitting. Parameter space bifurcation diagrams for the equilibria are drawn in the three-dimensional space of damage, splitting, and fusion, and solutions of the equations (i.e., the outcomes of the competition) are described in terms of them. It turns out that those three parameters suffice to give an essentially complete description of the qualitative behavior possible, since one parameter can be scaled out of the equations we ultimately consider, and the other permits generic analysis, for the range of parameter values of interest, at a fixed value of that parameter. Each type of cell has a region of the parameter space that it occupies exclusively (given its initial presence in the competition). The haploid can win only in environments characterized by low damage (relative to mortality), while the diploid can win only in environments characterized by high damage (relative to mortality). However, the sexual may outcompete either of the asexuals in those domains assuming that the parameters of the sexual cycle are adjusted appropriately. In general, only a single type of cell occupies a given portion of the space. We find, however, that the competitive coexistence of a diploid and a sexual is possible in spite of the fact that they are competing for a single resource (nucleotide building blocks). This coexistence is the result of an overactive sexual cycle and so would presumably be selected against. (C) 1995 Academic Press, Inc.
• Bernstein, H., Byerly, H. C., Hopf, F. A., & Michod, R. E. (1984). Origin of sex. Journal of Theoretical Biology, 110(3), 323-351.
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  PMID: 6209512;Abstract: The competitive advantage of sex consists in being able to use redundancy to recover lost genetic information while minimizing the cost of redundancy. We show that the major selective forces acting early in evolution lead to RNA protocells in which each protocell contains one genome, since this maximizes the growth rate. However, damages to the RNA which block replication and failure of segregation make it advantageous to fuse periodically with another protocell to restore reproductive ability. This early, simple form of genetic recovery is similar to that occurring in extant segmented single stranded RNA viruses. As duplex DNA became the predominant form of the genetic material, the mechanism of genetic recovery evolved into the more complex process of recombinational repair, found today in a range of species. We thus conclude that sexual reproduction arose early in the evolution of life and has had a continuous evolutionary history. We cite reasons to reject arguments for gaps in the evolutionary sequence of sexual reproduction based on the presumed absence of sex in the cyanobacteria. Concerning the maintenance of the sexual cycle among current organisms, we take care to distinguish between the recombinational and outbreeding aspects of the sexual cycle. We argue that recombination, whether it be in outbreeding organisms, self-fertilizing organisms or automictic parthenogens, is maintained by the advantages of recombinational repair. We also discuss the role of DNA repair in maintaining the outbreeding aspects of the sexual cycle. © 1984 Academic Press Inc. (London) Ltd.
• Durand, P. M., Rashidi, A., & Michod, R. E. (1984). How an Organism Dies Affects the Fitness of Its Neighbors. AMERICAN NATURALIST, 177(2), 224-232.
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  Programmed cell death (PCD), a genetically regulated cell suicide program, is ubiquitous in the living world. In contrast to multicellular organisms, in which cells cooperate for the good of the organism, in unicells the cell is the organism and PCD presents a fundamental evolutionary problem. Why should an organism actively kill itself as opposed to dying ill a nonprogrammed way? Proposed arguments vary from PCD in unicells being maladaptive to the assumption that it is an extreme form of altruism. To test whether PCD could be beneficial to nearby cells, we induced programmed and nonprogrammed death in the unicellular green alga Chlamydomonas reinhardtii. Cellular contents liberated during non-PCD are detrimental to others, while the contents released during PCD are beneficial. The number of cells in growing cultures was used to measure fitness. Thermostability studies revealed that the beneficial effect of the PCD supernatant most likely involves simple heat-stable biomolecules. Non-PCD supernatant contains heat-sensitive molecules like cellular proteases and chlorophyll. These data indicate that the mode of death affects the origin and maintenance of PCD. The way in which an organism dies can have beneficial or deleterious effects on the fitness of its neighbors.
• Bernstein, H., Byerly, H. C., Hopf, F. A., Michod, R. A., & Vemulapalli, G. K. (1983). The Darwinian dynamic ( evolution).. Quarterly Review of Biology, 58(2), 185-207.
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  Abstract: The evolution of order in living systems and certain nonliving physical systems obeys a common fundamental principle, here called the Darwinian dynamic. Such ordered systems deviate greatly from the thermodynamic equiprobability rule. Specifically, the fitness of an RNA replicator (its per capita rate of increase) is shown to be a function of adaptive capacities which are intrinsic (in the sense that they are determined by the nucleotide sequence) and of the availability of resources.-from Authors
• Ferriere, R., & Michod, R. (1983). The evolution of cooperation in spatially heterogeneous populations. AMERICAN NATURALIST, 147(5), 692-717.
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  A challenging problem in sociobiology is to understand the emergence of cooperation in a nonsocial world. Recent models of the iterated Prisoner's Dilemma (IPD) game conclude that population mixing due to individual mobility limits cooperation; however, these models represent space only implicitly. Here we develop a dynamical IPD model where temporal and spatial variations in the population are explicitly considered. Our model accounts for the stochastic motion of individuals and the inherent nonrandomness of local interactions. By deriving a spatial version of Hamilton's rule, we find that a threshold level of mobility in selfish always-defect (AD) players is required to beget invasion by social ''tit for tat'' (TFT) players. Furthermore, the level of mobility of successful TFT newcomers must be approximately equal to or somewhat higher than that of resident defectors. Significant mobility promotes the assortment of TFT pioneers on the front of invasion and of AD intruders in the core of a cooperative cluster. It also maximizes the likelihood of TFT retaliation. Once this first step whereby TFT takes over AD is completed, more generous and perhaps more suspicious strategies may outperform and displace TFT. We derive the conditions under which this continued evolution of more robust cooperative strategies occurs.
• MICHOD, R. (1983). POPULATION BIOLOGY OF THE 1ST REPLICATORS - ON THE ORIGIN OF THE GENOTYPE, PHENOTYPE AND ORGANISM. AMERICAN ZOOLOGIST, 23(1), 5-14.
• Michod, R. E. (1983). Population biology of the first replicators: On the origin of the genotype, phenotype and organism. Integrative and Comparative Biology, 23(1), 5-14.
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  Abstract: Prebiotic synthesis of short length macromolecules from precursor molecules results in a dynamic of spontaneous creation, which allows for growth from zero density. At this prereplicator stage in the evolution of life there is no life history, since the birth and death processes are intimately coupled through the physical chemistry of a single reaction. With the emergence of nonenzymatic, template-directed replication, the birth and death processes could diverge for the first time, since selection could act differently on the birth and death rates of the replicating molecule. Thus, with replication, natural selection and life-history evolution began. The genotype, or nucleotide sequence, of the replicating molecule gave rise to several phenotypic properties, the most important of which was its three-dimensional structure which in turn affected the birth and death processes. However, at this stage of nonenzymatic template replication, the phenotype was the physical structure of the genotype, nothing more: For the divergence of the phenotype from the genotype it was necessary for the replicator to produce a protein. It is shown here that the evolution of enzyme production is facilitated by the existence of population structure in the distribution of the macromolecules associated with replication. Initially, this structure was created passively by the localization of the macromolecules in rock crevices, suspended water droplets, etc. Ultimately, the replicator along with its proteins were localized in a protocellular structure and this became the first organism. Thus, initially, the organism was one extreme of the population structure of the macromolecules associated with life. The organism was the culmination of the encapsulation phase of evolution which proceeded through initial phases of passive localization. © 1983 by the American Society of Zoologists.
• Michod, R. E. (1983). Population biology of the first replicators: on the origin of the genotype, phenotype and organism.. American Zoologist, 23(1), 5-14.
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  Abstract: Prebiotic synthesis of short length macromolecules from precursor molecules results in a dynamic of spontaneous creation, which allows for growth from zero density. At this prereplicator stage in the evolution of life there is no life history, since the birth and death processes are intimately coupled through the physical chemistry of a single reaction. With the emergence of nonenzymatic, template-directed replication, the birth and death processes could diverge for the first time, since selection could act differently on the birth and death rates of the replicating molecule. Thus, with replication, natural selection and life-history evolution began. The genotype, or nucleoitide sequence, of the replicating molecule gave rise to several phenotypic properties, the most important of which was its 3-dimensional structure which in turn affected the birth and death processes. For divergence of the phenotype from the genotype it was necessary for the replicator to produce a protein. The evolution of enzyme production is facilitated by the existence of population structure in the distribution of the macromolecules associated with replication. The organism was one extreme of the population structure of the macromolecules associated with life. The organism was the culmination of the encapsulation phase of evolution which proceeded through initial phases of passive localization. -from Author
• Brown, J. S., Sanderson, M. J., & Michod, R. E. (1982). Evolution of social behavior by reciprocation. Journal of Theoretical Biology, 99(2), 319-339.
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  Abstract: A general model is presented for the evolution of social behavior by reciprocation. The results of our model apply to social traits which are transmitted from one generation to the next by a process which guarantees that the frequency of the trait in one generation is directly related to its fitness in the preceding generation. The basic parameters of the model are α, the number of interactions per generation, and β, the number of these interactions which are with individuals who are perceived as strangers. It is shown that so long as α/β can be made large, social reciprocation may increase when arbitrarily rare even in the absence of population structure. This conclusion appears to be at odds with several recent investigations of Axelrod & Hamilton (1981) and Boorman & Levitt (1980). We use our model to reconcile these various approaches. By casting Axelrod & Hamilton's (1981) single-partner model in terms of the general parameters, α and β, we show that social reciprocation can increase when arbitrarily rare in a homogeneous population dominated by non-cooperators. Using a gene frequency approach, Boorman & Levitt (1973, 1980) demonstrated the existence of a selection threshold in frequency of the social trait, which must be surmounted for social reciprocation to increase. We show our analysis of reciprocation to be consistent with Boorman and Levitt's result, since for our general model the cost to the social individuals of learning the non-social's identity goes to zero as the ratio α/β gets large. We also use our general model to study two multi-partner models not considered elsewhere, which differ in regards to the memory capabilities assigned to the organism. Finally we use our model to compare directly the evolution of social behavior by reciprocation with the main alternate hypothesis, kin selection. We show that an act which accrues some cost -c to the fitness of the donor while benefiting a recipient by b, will increase in frequency so long as c/b < Φ (equation (30)), where Φ is defined as the "coefficient of reciprocation" or probability that a cooperative act is reciprocated. By comparing the coefficient of reciprocation with the coefficient of relatedness of kin selection, direct comparisons of the two hypotheses may be made. © 1982.
• MICHOD, R., & HASSON, O. (1982). ON THE EVOLUTION OF RELIABLE INDICATORS OF FITNESS. AMERICAN NATURALIST, 135(6), 788-808.
• Michod, R. E. (1982). The theory of kin selection.. Annual review of ecology and systematics. Volume 13, 23-55.
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  Abstract: Constructs a theoretical framework within which various models relating to kin selection can be placed in perspective. To evolve by kin selection a genetic trait expressed by one individual (actor) must affect the genotypic fitness of one or more other individuals who are genetically related to the actor in a non-random way at the loci determining the trait. Comments on this definition range over altruism, parental care and social selection. Relationships are shown between kin selection and frequency-dependent selection, individual selection and group selection. Discussion continues to include formal relations of the family-structured model to the identity coefficient model; parental manipulation; effects of inbreeding; and Hamilton's rule (for spread of an altrustic trait) and inclusive fitness.-P.J.Jarvis
• Michod, R., Viossat, Y., Solari, C., Hurand, M., & Nedelcu, A. (1982). Life-history evolution and the origin of multicellularity. JOURNAL OF THEORETICAL BIOLOGY, 239(2), 257-272.
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  The fitness of an evolutionary individual can be understood in terms of its two basic components: survival and reproduction. As embodied in current theory, trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. Here, we argue that the evolution of germ-soma specialization and the emergence of individuality at a new higher level during the transition from unicellular to multicellular organisms are also consequences of trade-offs between the two components of fitness-survival and reproduction. The models presented here explore fitness trade-offs at both the cell and group levels during the unicellular-multicellular transition. When the two components of fitness negatively covary at the lower level there is an enhanced fitness at the group level equal to the covariance of components at the lower level. We show that the group fitness trade-offs are initially determined by the cell level trade-offs. However, as the transition proceeds to multicellularity, the group level trade-offs depart from the cell level ones, because certain fitness advantages of cell specialization may be realized only by the group. The curvature of the trade-off between fitness components is a basic issue in life-history theory and we predict that this Curvature is concave in single-celled organisms but becomes increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the initial cost of reproduction to Survival which increases as group size increases. To illustrate the principles and conclusions of the model, we consider aspects of the biology of the volvocine green algae, which contain both unicellular and multicellular members. (C) 2005 Elsevier Ltd. All rights reserved.
• Nedelcu, A. M., & Michod, R. E. (1982). The evolutionary origin of an altruistic gene. MOLECULAR BIOLOGY AND EVOLUTION, 23(8), 1460-1464.
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  Although the conditions favoring altruism are being increasingly understood, the evolutionary origins of the genetic basis for this behavior remain elusive. Here, we show that reproductive altruism (i.e., a sterile soma) in the multicellular green alga, Volvox carteri, evolved via the co-option of a life-history gene whose expression in the unicellular ancestor was conditioned on an environmental cue (as an adaptive strategy to enhance survival at an immediate cost to reproduction) through shifting its expression from a temporal (environmentally induced) into a spatial (developmental) context. The gene belongs to a diverged and structurally heterogeneous multigene family sharing a SAND-like domain (a DNA-binding module involved in gene transcription regulation). To our knowledge, this is the first example of a social gene specifically associated with reproductive altruism, whose origin can be traced back to a solitary ancestor. These findings complement recent proposals that the differentiation of sterile castes in social insects involved the co-option of regulatory networks that control sequential shifts between phases in the life cycle of solitary insects.
• Toro, M., Abugov, R., Charlesworth, B., & Michod, R. E. (1982). Exact versus heuristic models of kin selection. Journal of Theoretical Biology, 97(4), 699-713.
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  PMID: 7154687;Abstract: This paper examines the conditions under which the classical inclusive fitness formulation of Hamilton (1964) provides an adequate approximation to the dynamics of gene frequency change and to conditions for genetic equilibrium, in the "additive" model of altruism between sibs of Uyenoyama and Feldman (1981). It is concluded that the classical formulation is adequate, provided that either the effect of the gene on the probability of behaving altruistically is low or the costs and benefits of altruism are small, unless the benefit/cost ratio k is very close to 2, the value that must be exceeded for altruism to be favoured. In addition, the gene for altruism must be underdominant, recessive or partially recessive in its effect on the probability of behaving altruistically, for the inclusive fitness predictions to break down significantly. © 1982.
• Abugov, R., & Michod, R. E. (1981). On the relation of family structured models and inclusive fitness models for kin selection. Journal of Theoretical Biology, 88(4), 743-754.
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  PMID: 7266013;Abstract: The concept of inclusive fitness plays a key role in much of sociobiology. Yet most theoretical studies concerning the evolution of social behavior circumvent inclusive fitness by mobilizing the concept of frequencydependent individual fitness. Given certain assumptions, it is shown that models based on these two different concepts are dynamically equivalent. The models do differ, however, in bookkeeping methods which are advantageous under different circumstances. A knowledge of these circumstances should prove of value to students of social behavior. © 1981.
• MICHOD, R. (1981). POSITIVE HEURISTICS IN EVOLUTIONARY BIOLOGY. BRITISH JOURNAL FOR THE PHILOSOPHY OF SCIENCE, 32(1), 1-36.
• Michod, R. E. (1981). Positive heuristics in evolutionary biology. British Journal for the Philosophy of Science, 32(1), 1-36.
• Solari, C., Ganguly, S., Kessler, J., Michod, R., & Goldstein, R. (1981). Multicellularity and the functional interdependence of motility and molecular transport. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 103(5), 1353-1358.
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  Benefits, costs, and requirements accompany the transition from motile totipotent unicellular organisms to multicellular organisms having cells specialized into reproductive (germ) and vegetative (sterile soma) functions such as motility. In flagellated colonial organisms such as the volvocalean green algae, organized beating by the somatic cells' flagella yields propulsion important in phototaxis and chemotaxis. It has not been generally appreciated that for the larger colonies flagellar stirring of boundary layers and remote transport are fundamental for maintaining a sufficient rate of metabolite turnover, one not attainable by diffusive transport alone. Here, we describe experiments that quantify the role of advective dynamics in enhancing productivity in germ soma-differentiated colonies. First, experiments with suspended deflagellated colonies of Volvox carteri show that forced advection improves productivity. Second, particle imaging velocimetry of fluid motion around colonies immobilized by micropipette aspiration reveals flow fields with very large characteristic velocities U extending to length scales exceeding the colony radius R. For a typical metabolite diffusion constant D, the associated Peclet number Pe = 2UR/D >> 1, indicative of the dominance of advection over diffusion, with striking augmentation at the cell division stage. Near the colony surface, flows generated by flagella can be chaotic, exhibiting mixing due to stretching and folding. These results imply that hydrodynamic transport external to colonies provides a crucial boundary condition, a source for supplying internal diffusional dynamics.
• MICHOD, R., & ANDERSON, W. (1980). MEASURES OF GENETIC-RELATIONSHIP AND THE CONCEPT OF INCLUSIVE FITNESS. AMERICAN NATURALIST, 114(5), 637-647.
• Michod, R. (1980). Cooperation and conflict in the evolution of individuality .2. Conflict mediation. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 263(1372), 813-822.
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  Evolutionary transitions in the units of selection require the promotion of cooperation and the regulation of conflict among the lower level units. For multicellular organisms to emerge as a new unit of selection, the selfish tendencies of their component cells had to be controlled. Theoretical results indicate organisms may regulate this internal conflict and competition in several ways: by reducing the somatic mutation rate, by sequestering cells in a germ line and by directly reducing the benefits to cells of defecting.
• Michod, R. E. (1980). Evolution of interactions in family-structured populations: Mixed mating models. Genetics, 96(1), 275-296.
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  PMID: 17249062;PMCID: PMC1214295;
• Michod, R. E., & Abugov, R. (1980). Adaptive topography in family-structured models of kin selection. Science, 210(4470), 667-669.
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  PMID: 17815158;
• Michod, R. E., & Hamilton, W. D. (1980). Coefficients of relatedness in sociobiology. Nature, 288(5792), 694-697.
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  Abstract: A much-discussed, quantitative criterion for the spread of an altruistic gene is Hamilton's rule1,2c/b < R (1)where c and b are additive decrement and increment to fitness of altruist and recipient, respectively, and R is a measure of genetic relatedness between the two individuals. When rearranged as -c.1+b.R > 0, the rule can be interpreted as requiring that the gene-caused action increase the 'inclusive fitness' of the actor. Since its introduction, Hamilton's rule and the attendant concept of inclusive fitness have gained increasing acceptance and use among biologists and have become integral in the field now named sociobiology. However, the essentially heuristic reasoning used in deriving these concepts, along with the lack of a complete specification even in the original outbred model2, have led to many investigations into the population genetical underpinnings of Hamilton's rule3-18. On the basis of these considerations, several reports 3,10,12,13,18 have proposed new formulae for R. These formulae have no obvious relation to each other or to the coefficients originally suggested by Hamilton. This proliferation of coefficients is undoubtedly confusing to many and the net effect may be to generate distrust both of the rule and of the notion of inclusive fitness. Our purpose here is to show that these various formulae for R (refs 3,10,12,13,18), although independently derived, are actually the same. © 1980 Nature Publishing Group.
• Michod, R., Nedelcu, A., & Roze, D. (1980). Cooperation and conflict in the evolution of individuality IV. Conflict mediation and evolvability in Volvox carteri. BIOSYSTEMS, 69(2-3), 95-114.
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  The continued well being of evolutionary individuals (units of selection and evolution) depends upon their evolvability, that is their capacity to generate and evolve adaptations at their level of organization, as well as their longer term capacity for diversifying into more complex evolutionary forms. During a transition from a lower- to higher-level individual, such as the transition between unicellular and multicellular organisms, the evolvability of the lower-level (cells) must be restricted, while the evolvability of the new higher-level unit (multicellular organism) must be enhanced. For these reasons, understanding the factors leading to an evolutionary transition should help us to understand the factors underlying the emergence of evolvability of a new evolutionary unit. Cooperation among lower-level units is fundamental to the origin of new functions in the higher-level unit. Cooperation can produce a new more complex evolutionary unit, with the requisite properties of heritable fitness variations, because cooperation trades fitness from a lower-level (the costs of cooperation) to the higher-level (the benefits for the group). For this reason, the evolution of cooperative interactions helps us to understand the origin of new and higher-levels of fitness and organization. As cooperation creates a new level of fitness, it also creates the opportunity for conflict between levels of selection, as deleterious mutants with differing effects at the two levels arise and spread. This conflict can interfere with the evolvability of the higher-level unit, since the lower and higher-levels of selection will often "disagree" on what adaptations are most beneficial to their respective interests. Mediation of this conflict is essential to the emergence of the new evolutionary unit and to its continued evolvability. As an example, we consider the transition from unicellular to multicellular organisms and study the evolution of an early-sequestered germ-line in terms of its role in mediating conflict between the two levels of selection, the cell and the cell group. We apply our theoretical framework to the evolution of germ/soma differentiation in the green algal group Volvocales. In the most complex member of the group, Volvox carteri, the potential conflicts among lower-level cells as to the "right" to reproduce the higher-level individual (i.e. the colony) have been mediated by restricting immortality and totipotency to the germ-line. However, this mediation, and the evolution of an early segregated germ-line, was achieved by suppressing mitotic and differentiation capabilities in all post-embryonic cells. By handicapping the soma in this way, individuality is ensured, but the solution has affected the long-term evolvability of this lineage. We think that although conflict mediation is pivotal to the emergence of individuality at the higher-level, the way in which the mediation is achieved can greatly affect the longer-term evolvability of the lineage. (C) 2002 Elsevier Science Ireland Ltd. All rights reserved.
• MICHOD, R., MICHOD, R., & MICHOD, R. (1979). GENETIC-ASPECTS OF KIN SELECTION - EFFECTS OF INBREEDING. JOURNAL OF THEORETICAL BIOLOGY, 81(2), 223-233.
• Michod, R. (1979). Genetical aspects of kin selection: Effects of inbreeding. Journal of Theoretical Biology, 81(2), 223-233.
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  PMID: 537369;Abstract: Hamilton's c/b < "r" rule is an important tool in sociobiological research and clearly functions as a "positive heuristic", sensu Lakatos (1970). This paper examines the theoretical underpinnings of this rule in population genetics when inbreeding is taken into account. The model used is an extension of Charnov (1977) and assumes that the altruistic gene codes for a behavior between inbred individuals of a fixed genetic relationship. No consideration is given to the population or mating system processes which give rise to this relationship. It is shown that in inbred populations with weak selection the right-hand side of Hamilton's rule depends upon gene frequency and dominance as well as the degree of genetic relationship between the individuals involved. Because of this dependence, stable polymorphisms in altruistic and non-altruistic alleles are possible for certain ranges of c/b ratios. Another consequence is that the more dominant the altruistic gene, the easier it is for it to invade a population, but the harder it is for it to increase to high frequencies. In the special case when the individuals involved are inbred to the same extent and gene effects are additive, the RHS of the rule is independent of gene frequency and equals bYX and rYX: respectively Hamilton's regression coefficient of relatedness and Wright's correlation coefficient of relationship. © 1979.
• Solari, C. A., Drescher, K., Ganguly, S., Kessler, J. O., Michod, R. E., & Goldstein, R. E. (1979). Flagellar phenotypic plasticity in volvocalean algae correlates with Peclet number. JOURNAL OF THE ROYAL SOCIETY INTERFACE, 8(63), 1409-1417.
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  Flagella-generated fluid stirring has been suggested to enhance nutrient uptake for sufficiently large micro-organisms, and to have played a role in evolutionary transitions to multicellularity. A corollary to this predicted size-dependent benefit is a propensity for phenotypic plasticity in the flow-generating mechanism to appear in large species under nutrient deprivation. We examined four species of volvocalean algae whose radii and flow speeds differ greatly, with Peclet numbers (Pe) separated by several orders of magnitude. Populations of unicellular Chlamydomonas reinhardtii and one-to eight-celled Gonium pectorale (Pe similar to 0.1-1) and multicellular Volvox carteri and Volvox barberi (Pe similar to 100) were grown in diluted and undiluted media. For C. reinhardtii and G. pectorale, decreasing the nutrient concentration resulted in smaller cells, but had no effect on flagellar length and propulsion force. In contrast, these conditions induced Volvox colonies to grow larger and increase their flagellar length, separating the somatic cells further. Detailed studies on V. carteri found that the opposing effects of increasing beating force and flagellar spacing balance, so the fluid speed across the colony surface remains unchanged between nutrient conditions. These results lend further support to the hypothesized link between the Peclet number, nutrient uptake and the evolution of biological complexity in the Volvocales.
• Solari, C., Kessler, J., & Michod, R. (1979). A hydrodynamics approach to the evolution of multicellularity: Flagellar motility and germ-soma differentiation in volvocalean green algae. AMERICAN NATURALIST, 167(4), 537-554.
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  During the unicellular-multicellular transition, there are opportunities and costs associated with larger size. We argue that germ-soma separation evolved to counteract the increasing costs and requirements of larger multicellular colonies. Volvocalean green algae are uniquely suited for studying this transition because they range from unicells to multicellular individuals with germ-soma separation. Because Volvocales need flagellar beating for movement and to avoid sinking, their motility is modeled and analyzed experimentally using standard hydrodynamics. We provide comparative hydrodynamic data of an algal lineage composed of organisms of different sizes and degrees of complexity. In agreement with and extending the insights of Koufopanou, we show that the increase in cell specialization as colony size increases can be explained in terms of increased motility requirements. First, as colony size increases, soma must evolve, the somatic-to-reproductive cell ratio increasing to keep colonies buoyant and motile. Second, increased germ-soma specialization in larger colonies increases motility capabilities because internalization of non-flagellated germ cells decreases colony drag. Third, our analysis yields a limiting maximum size of the volvocalean spheroid that agrees with the sizes of the largest species known. Finally, the different colony designs in Volvocales reflect the trade-offs between reproduction, colony size, and motility.
• Anderson, W. W., Ayala, F. J., & Michod, R. E. (1977). Chromosomal and allozymic diagnosis of three species of Drosophila. Drosophila pseudoobscura, D. persimilis, and D. miranda. Journal of Heredity, 68(2), 71-74.
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  PMID: 874309;

Proceedings Publications

• MICHOD, R., WOJCIECHOWSKI, M., HOELZER, M., CLEGG, M., & OBRIEN, S. (2003). EVOLUTION OF SEX IN PROKARYOTES. In MOLECULAR EVOLUTION, 122, 135-144.
• Michod, R., & Hammerstein, P. (1983). Cooperation and conflict mediation during the origin of multicellularity. In GENETIC AND CULTURAL EVOLUTION OF COOPERATION, 291-307.
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  The basic problem in an evolutionary transition is to understand how a group of individuals becomes a new kind of individual, having heritable variation in fitness at the new level of organization. We see the formation of cooperative interactions among lower-level individuals as a necessary step in evolutionary transitions; only cooperation transfers fitness from lower levels (costs to group members) to higher levels (benefits to the group). As cooperation creates a new level of fitness, it creates the opportunity for conflict between the new level and the lower level. Fundamental to the emergence of a new higher-level individual is the mediation of conflict among lower-level individuals in favor of the higher-level unit. We define a conflict mediator as a feature of the cell group (the emerging multicellular organism) that restricts the opportunity for fitness variation at the lower level (cells) and/or enhances the variation in fitness at the higher level (the cell group). There is abundant evidence that organisms are endowed with just such traits and numerous examples are reviewed here from the point of view of a population genetic model of conflict mediation. Our model considers the evolution of genetic modifiers that mediate conflict between the cell and the cell group. These modifiers alter the parameters of development, or rules of formation, of cell groups. By sculpting the fitness variation and opportunity for selection at the two levels, conflict modifiers create new functions at the organism level. An organism is more than a group of cooperating cells related by common descent and requires adaptations that regulate conflict within itself. Otherwise, its individuality and continued evolvability is frustrated by the creation of within-organism variation and conflict between levels of selection. Conflict leads to greater individuality and harmony for the organism through the evolution of adaptations that reduce it.
• Lachmann, M., Blackstone, N., Haig, D., Kowald, A., Michod, R., Szathmary, E., Werren, J., Wolpert, L., & Hammerstein, P. (1982). Group report: Cooperation and conflict in the evolution of genomes, cells, and multicellular organisms. In GENETIC AND CULTURAL EVOLUTION OF COOPERATION, 327-356.

Reviews

• MICHOD, R. (2008. MOLECULAR THEORY OF EVOLUTION - OUTLINE OF A PHYSICOCHEMICAL THEORY OF THE ORIGIN OF LIFE - KUPPERS,BO(pp 171-172).
• BERNSTEIN, H., HOPF, F., & MICHOD, R. (2003. THE MOLECULAR-BASIS OF THE EVOLUTION OF SEX(pp 323-370).
• Michod, R., & Roze, D. (2003. Cooperation and conflict in the evolution of multicellularity(pp 1-7).
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  Multicellular organisms probably originated as groups of cells formed in several ways, including cell proliferation from a group of founder cells and aggregation. Cooperation among cells benefits the group, but may be costly (altruistic) or beneficial (synergistic) to individual cooperating cells. In this paper, we study conflict mediation, the process by which genetic modifiers evolve that enhance cooperation by altering the parameters of development or rules of formation of cell groups. We are particularly interested in the conditions under which these modifiers lead to a new higher-level unit of selection with increased cooperation among group members and heritable variation in fitness at the group level. By sculpting the fitness variation and opportunity for selection at the two levels, conflict modifiers create new functions at the organism level. An organism is more than a group of cooperating cells related by common descent; organisms require adaptations that regulate conflict within. Otherwise their continued evolution is frustrated by the: creation of within-organism variation and conflict between levels of selection. The evolution of conflict modifiers is a necessary prerequisite to the emergence of individuality and the continued well being of the organism. Conflict leads - through the evolution of adaptations that reduce it - to greater individuality and harmony for the organism.
• MICHOD, R. (1996. THE THEORY OF KIN SELECTION(pp 23-55).
• MICHOD, R. (1991. THE EXTENDED PHENOTYPE - THE GENE AS THE UNIT OF SELECTION - DAWKINS,R(pp 525-526).
• MICHOD, R. (1990. THE GENETICS OF ALTRUISM - BOORMAN,SA, LEVITT,PR(pp 308-309).
• SANDERSON, M., & MICHOD, R. (1984. CULTURAL TRANSMISSION AND EVOLUTION - A QUANTITATIVE APPROACH - CAVALLISFORZA,LL, FELDMAN,M(pp 956-958).
• BERNSTEIN, H., BYERLY, H., HOPF, F., & MICHOD, R. (1981. THE EVOLUTIONARY ROLE OF RECOMBINATIONAL REPAIR AND SEX(pp 1-28).
• MICHOD, R. (1980. ECOLOGICAL GENETICS - REAL,LA(pp 468-470).

Others

• Michod, R. (2008, MAR-APR). Blood feud - Richard E. Michod replies. SCIENCES-NEW YORK.
• BYERLY, H., & MICHOD, R. (2006, JAN). FITNESS AND EVOLUTIONARY EXPLANATION - A RESPONSE. BIOLOGY & PHILOSOPHY.
• Durand, P. M., & Michod, R. E. (2006, JUN). GENOMICS IN THE LIGHT OF EVOLUTIONARY TRANSITIONS. EVOLUTION.
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  Molecular biology has entrenched the gene as the basic hereditary unit and genomes are often considered little more than collections of genes. However, new concepts and genomic data have emerged, which suggest that the genome has a unique place in the hierarchy of life. Despite this, a framework for the genome as a major evolutionary transition has not been fully developed. Instead, genome origin and evolution are frequently considered as a series of neutral or nonadaptive events. In this article, we argue for a Darwinian multilevel selection interpretation for the origin of the genome. We base our arguments on the multilevel selection theory of hypercycles of cooperative interacting genes and predictions that gene-level trade-offs in viability and reproduction can help drive evolutionary transitions. We consider genomic data involving mobile genetic elements as a test case of our view. A new concept of the genome as a discrete evolutionary unit emerges and the gene-genome juncture is positioned as a major evolutionary transition in individuality. This framework offers a fresh perspective on the origin of macromolecular life and sets the scene for a new, emerging line of inquiry-the evolutionary ecology of the genome.
• Abbot, P., Abe, J., Alcock, J., Alizon, S., Alpedrinha, J. A., Andersson, M., Andre, J., van Baalen, M., Balloux, F., Balshine, S., Barton, N., Beukeboom, L. W., Biernaskie, J. M., Bilde, T., Borgia, G., Breed, M., Brown, S., Bshary, R., Buckling, A., , Burley, N. T., et al. (1995, MAR 24). Inclusive fitness theory and eusociality. NATURE.
• Michod, R. (1986, MAR). Evolution of individuality. JOURNAL OF EVOLUTIONARY BIOLOGY.
• Ferriere, R., & Michod, R. E. (1985, MAR 24). Inclusive fitness in evolution. NATURE.
• Michod, R. E., & Herron, M. D. (1983, SEP). Cooperation and conflict during evolutionary transitions in individuality. JOURNAL OF EVOLUTIONARY BIOLOGY.
• Michod, R. (1977). John Maynard Smith. ANNUAL REVIEW OF GENETICS.
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  John Maynard Smith was one of the most original thinkers in evolutionary biology of the post neo-Darwinian synthesis age. He was able to define new problems with clarity and by doing so open up new research directions. He did this in a number of areas including game theory and evolution, the evolution of sex, animal behavior, evolutionary transitions and molecular evolution. Although he is best known for his research and his ideas, he was a great expositor and wrote many books, including introductory texts in the areas of evolution and genetics, ecology and mathematical modeling, as well as advanced expositions of research problems.