Lisa M Nagy
- Professor, Molecular and Cellular Biology
- Professor, Ecology and Evolutionary Biology
- Professor, Cellular and Molecular Medicine
- Professor, Entomology / Insect Science - GIDP
- Ph.D. Zoology
- University of Washington, Seattle, Washington, United States
- Team Award for Excellence in Teaching, Collaborative Learning Space Team
- Fall 2015
No activities entered.
Directed RsrchMCB 492 (Fall 2016)
Honors Independent StudyMCB 399H (Fall 2016)
ResearchMCB 900 (Fall 2016)
Special Tutoring WkshpMCB 497A (Fall 2016)
ThesisMCB 910 (Fall 2016)
Directed RsrchMCB 392 (Spring 2016)
Directed RsrchMCB 492 (Spring 2016)
Honors Independent StudyMCB 499H (Spring 2016)
Honors ThesisMCB 498H (Spring 2016)
Master's ReportABS 909 (Spring 2016)
Cell SystemsMCB 572A (Fall 2015)
Cell&Development BiologyMCB 305 (Fall 2015)
Directed RsrchMCB 392 (Fall 2015)
Directed RsrchMCB 492 (Fall 2015)
DissertationEIS 920 (Fall 2015)
Honors Independent StudyMCB 499H (Fall 2015)
Honors ThesisMCB 498H (Fall 2015)
Special Tutoring WkshpMCB 497A (Fall 2015)
Internship in Applied BiosciABS 593A (Summer I 2015)
Directed RsrchMCB 392 (Spring 2015)
Directed RsrchMCB 492 (Spring 2015)
DissertationEIS 920 (Spring 2015)
DissertationMCB 920 (Spring 2015)
Honors Independent StudyMCB 399H (Spring 2015)
Honors Independent StudyMCB 499H (Spring 2015)
Internship in Applied BiosciABS 593A (Spring 2015)
Lab Presentations & DiscussionMCB 696A (Spring 2015)
Master's ReportABS 909 (Spring 2015)
Cell SystemsMCB 572A (Fall 2014)
Cell&Development BiologyMCB 305 (Fall 2014)
DissertationEIS 920 (Fall 2014)
DissertationMCB 920 (Fall 2014)
Honors Independent StudyMCB 399H (Fall 2014)
Independent StudyMCB 599 (Fall 2014)
Internship in Applied BiosciABS 593A (Fall 2014)
Lab Presentations & DiscussionMCB 696A (Fall 2014)
Special Tutoring WkshpMCB 497A (Fall 2014)
Internship in Applied BiosciABS 593A (Summer I 2014)
Directed RsrchMCB 492 (Spring 2014)
DissertationMCB 920 (Spring 2014)
Honors Independent StudyECOL 399H (Spring 2014)
Honors Independent StudyMCB 399H (Spring 2014)
Lab Presentations & DiscussionMCB 696A (Spring 2014)
ResearchEIS 900 (Spring 2014)
ThesisBIOC 910 (Spring 2014)
Cell SystemsMCB 572A (Fall 2013)
Cell&Development BiologyMCB 305 (Fall 2013)
Directed RsrchMCB 492 (Fall 2013)
Honors Independent StudyECOL 399H (Fall 2013)
Honors Independent StudyMCB 399H (Fall 2013)
Independent StudyMCB 599 (Fall 2013)
Lab Presentations & DiscussionMCB 696A (Fall 2013)
ResearchMCB 900 (Fall 2013)
ThesisBIOC 910 (Fall 2013)
ResearchBIOC 900 (Summer I 2013)
- Nagy, L. M., Constantinou, S., Pace, R., Stangl, A. J., & Williams, T. A. (2016). Wnt repertoire and developmental expression patterns in the crustacean Thamnocephalus platyurus.. Evolution and Development, 18(5-6), 324-341. doi:10.1111/ede.12204
- Nagy, L. M., Pace, R., & Grbic, M. (2016). Composition and genomic organization of arthropod Hox clusters. EvoDevo, 7, 11. doi:10.1186/s1227-016-0048-4
- Nagy, L. M., Nakamoto, A., Hester, S. D., Williams, T. A., Matei, M. T., Constantinou, S. J., Blaine, W. G., & Tewksbury, A. B. (2015). Changing cell behaviours during beetle embryogenesis correlates with slowing of segmentation. Nature Communications, 6, 6635. doi:10.1038/ncomms7635
- Gharbiah, M., Nakamoto, A., Johnson, A. B., Lambert, J. D., & Nagy, L. M. (2014). Ilyanassa Notch signaling implicated in dynamic signaling between all three germ layers. The International journal of developmental biology, 58(6-7-8), 551-562.More infoTwo cells (3D and 4d) in the mud snail Ilyanassa obsoleta function to induce proper cell fate. In this study, we provide support for the hypothesis that Notch signaling in Ilyanassa obsoleta functions in inductive signaling at multiple developmental stages. The expression patterns of Notch, Delta and Suppressor of Hairless (SuH) are consistent with a function for Notch signaling in endoderm formation, the function of 3D/4d and the sublineages of 4d. Veligers treated with DAPT show a range of defects that include a loss of endodermal structures, and varying degrees of loss of targets of 4d inductive signaling. Veligers that result from injection of Ilyanassa Delta siRNAi in general mimic the defects observed in the DAPT treated larvae. The most severe DAPT phenotypes mimic early ablations of 4d. However, the early specification of 4d itself appears normal and MAPK activation in both 3D/4d and the micromeres, which are known to activate MAPK as a result of 3D/4d induction, are normal in DAPT treated larvae. Treating larvae at successively later timepoints with DAPT suggests that Notch/Delta signaling is not only required during early 4d inductive signaling, but during subsequent stages of cell fate determination as well. Based on our results, combined with previous reports implicating the endoderm in maintaining induced fate specification in Ilyanassa, we propose a speculative model that Notch signaling is required to specify endoderm fates and 4d sublineages, as well as to maintain cell fates induced by 4d.
- Hester, S. D., Buxner, S. R., Elfring, L., & Nagy, L. M. (2014). Integrating quantitative thinking into an introductory biology course improves students’ mathematical reasoning in biological contexts. CBE Life Sciences Education, 13(1), 54-64.
- Nagy, L. M., & Williams, T. A. (2014). EvoDevo and the promise of Understanding Morphological Transitions in Evolution.. Ann. Missouri Bot. Gard, 99.
- Pace, R. M., Eskridge, P. C., Grbić, M., & Nagy, L. M. (2014). Evidence for the plasticity of arthropod signal transduction pathways. Development genes and evolution, 224(4-6), 209-22.More infoMetazoans are known to contain a limited, yet highly conserved, set of signal transduction pathways that instruct early developmental patterning mechanisms. Genomic surveys that have compared gene conservation in signal transduction pathways between various insects and Drosophila support the conclusion that these pathways are conserved in evolution. However, the degree to which individual components of signal transduction pathways vary among more divergent arthropods is not known. Here, we report our results of a survey of the genome of the two-spotted spider mite Tetranychus urticae, using a set of 294 Drosophila orthologs of genes that function in signal transduction. We find a third of all genes surveyed absent from the spider mite genome. We also identify several novel duplications that have not been previously reported for a chelicerate. In comparison with previous insect surveys, Tetranychus contains a decrease in overall gene conservation, as well as an unusual ratio of ligands to receptors and other modifiers. These findings suggest that gene loss and duplication among components of signal transduction pathways are common among arthropods and suggest that signal transduction pathways in arthropods are more evolutionarily labile than previously hypothesized.
- Gharbiah, M., Nakamoto, A., & Nagy, L. M. (2013). Analysis of ciliary band formation in the mollusc Ilyanassa obsoleta. Development Genes and Evolution, 223(4), 225-235.More infoPMID: 23592252;Abstract: Two primary ciliary bands, the prototroch and metatroch, are required for locomotion and in the feeding larvae of many spiralians. The metatroch has been reported to have different cellular origins in the molluscs Crepidula fornicata and Ilyanassa obsoleta, as well as in the annelid Polygordius lacteus, consistent with multiple independent origins of the spiralian metatroch. Here, we describe in further detail the cell lineage of the ciliary bands in the gastropod mollusc I. obsoleta using intracellular lineage tracing and the expression of an acetylated tubulin antigen that serves as a marker for ciliated cells. We find that the I. obsoleta metatroch is formed primarily by third quartet derivatives as well as a small number of second quartet derivatives. These results differ from the described metatrochal lineage in the mollusc C. fornicata that derives solely from the second quartet or the metatrochal lineage in the annelid P. lacteus that derives solely from the third quartet. The present study adds to a growing body of literature concerning the evolution of the metatroch and the plasticity of cell fates in homologous micromeres in spiralian embryos. © 2013 Springer-Verlag Berlin Heidelberg.
- Williams, T., Blachuta, B., Hegna, T. A., & Nagy, L. M. (2012). Decoupling elongation and segmentation: Notch involvement in anostracan crustacean segmentation. Evolution and Development, 14(4), 372-382.More infoPMID: 22765208;Abstract: Repeated body segments are a key feature of arthropods. The formation of body segments occurs via distinct developmental pathways within different arthropod clades. Although some species form their segments simultaneously without any accompanying measurable growth, most arthropods add segments sequentially from the posterior of the growing embryo or larva. The use of Notch signaling is increasingly emerging as a common feature of sequential segmentation throughout the Bilateria, as inferred from both the expression of proteins required for Notch signaling and the genetic or pharmacological disruption of Notch signaling. In this study, we demonstrate that blocking Notch signaling by blocking γ-secretase activity causes a specific, repeatable effect on segmentation in two different anostracan crustaceans, Artemia franciscana and Thamnocephalus platyurus. We observe that segmentation posterior to the third or fourth trunk segment is arrested. Despite this marked effect on segment addition, other aspects of segmentation are unaffected. In the segments that develop, segment size and boundaries between segments appear normal, engrailed stripes are normal in size and alignment, and overall growth is unaffected. By demonstrating Notch involvement in crustacean segmentation, our findings expand the evidence that Notch plays a crucial role in sequential segmentation in arthropods. At the same time, our observations contribute to an emerging picture that loss-of-function Notch phenotypes differ significantly between arthropods suggesting variability in the role of Notch in the regulation of sequential segmentation. This variability in the function of Notch in arthropod segmentation confounds inferences of homology with vertebrates and lophotrochozoans. © 2012 Wiley Periodicals, Inc.
- Grbić, M., Leeuwen, T. V., Clark, R. M., Rombauts, S., Rouzé, P., Grbić, V., Osborne, E. J., Dermauw, W., Cao, P., Ortego, F., Hernández-Crespo, P., Diaz, I., Martinez, M., Navajas, M., Sucena, É., Magalhães, S., Nagy, L., Pace, R. M., Djuranović, S., , Smagghe, G., et al. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374), 487-492.More infoPMID: 22113690;Abstract: The spider mite Tetranychus urticae is a cosmopolitan agricultural pest with an extensive host plant range and an extreme record of pesticide resistance. Here we present the completely sequenced and annotated spider mite genome, representing the first complete chelicerate genome. At 90 megabases T. urticae has the smallest sequenced arthropod genome. Compared with other arthropods, the spider mite genome shows unique changes in the hormonal environment and organization of the Hox complex, and also reveals evolutionary innovation of silk production. We find strong signatures of polyphagy and detoxification in gene families associated with feeding on different hosts and in new gene families acquired by lateral gene transfer. Deep transcriptome analysis of mites feeding on different plants shows how this pest responds to a changing host environment. The T. urticae genome thus offers new insights into arthropod evolution and plant-herbivore interactions, and provides unique opportunities for developing novel plant protection strategies. © 2011 Macmillan Publishers Limited. All rights reserved.
- Nakamoto, A., Nagy, L. M., & Shimizu, T. (2011). Secondary embryonic axis formation by transplantation of D quadrant micromeres in an oligochaete annelid. Development, 138(2), 283-290.More infoPMID: 21148182;Abstract: Among spiral cleaving embryos (e.g. mollusks and annelids), it has long been known that one blastomere at the four-cell stage, the D cell, and its direct descendants play an important role in axial pattern formation. Various studies have suggested that the D quadrant acts as the organizer of the embryonic axes in annelids, although this has never been demonstrated directly. Here we show that D quadrant micromeres (2d and 4d) of the oligochaete annelid Tubifex tubifex are essential for embryonic axis formation. When 2d and 4d were ablated the embryo developed into a rounded cell mass covered with an epithelial cell sheet. To examine whether 2d and 4d are sufficient for axis formation they were transplanted to an ectopic position in an otherwise intact embryo. The reconstituted embryo formed a secondary embryonic axis with a duplicated head and/or tail. Cell lineage analyses showed that neuroectoderm and mesoderm along the secondary axis were derived from the transplanted D quadrant micromeres and not from the host embryo. However, endodermal tissue along the secondary axis originated from the host embryo. Interestingly, when either 2d or 4d was transplanted separately to host embryos, the reconstituted embryos failed to form a secondary axis, suggesting that both 2d and 4d are required for secondary axis formation. Thus, the Tubifex D quadrant micromeres have the ability to organize axis formation, but they lack the ability to induce neuroectodermal tissues, a characteristic common to chordate primary embryonic organizers.
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Fixation of Ilyanassa snail embryos and larvae. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147129;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Induction of larval metamorphosis in the snail Ilyanassa. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147127;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Isolation of genomic DNA from Ilyanassa snail larvae. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147130;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Obtaining Ilyanassa snail embryos. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147126;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Pressure injection of Ilyanassa snail embryos. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147128;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Rabinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). The snail Ilyanassa: A reemerging model for studies in development. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147120;
- Gharbiah, M., Cooley, J., Leise, E. M., Nakamoto, A., Robinowitz, J. S., Lambert, J. D., & Nagy, L. M. (2009). Isolating protein from Ilyanassa snail embryos. Cold Spring Harbor Protocols, 4(4).More infoPMID: 20147131;
- Nagy, L., & Grbić, M. (2009). Embryogenesis. Encyclopedia of Insects, 316-320.More infoAbstract: This chapter presents a generalized view of some of the more regular features of insect development. Embryogenesis is the process by which a larva or a juvenile is built from a single egg. The fertilized egg divides to produce hundreds of cells that grow, move, and differentiate into all the organs and tissues required to form a larva or juvenile. Embryogenesis is extremely diverse in different insect species. In some species, a single egg gives rise to several thousand larvae; in others, embryos devour their mothers before hatching. The most extreme variations are found among insects that parasitize other insects. Insect eggs are typically quite large, both in absolute dimensions and relative to maternal body size, and well provisioned with yolk. Eggs vary from about 0.02 to 20 mm in length. To prevent desiccation, they are covered by some of the most resistant and impenetrable egg coverings found in the animal kingdom. Egg contents are protected by a vitelline membrane and covered by an external hard shell, the chorion. © 2009 Elsevier Inc. All rights reserved.
- Nagy, L., Nagy, L., Gharbiah, M., Gharbiah, M., Cooley, J., Cooley, J., Leise, E. M., Leise, E. M., Nakamoto, A., Nakamoto, A., Rabinowitz, J. S., Rabinowitz, J. S., Lambert, J. D., Lambert, J. D., Nagy, L. M., & Nagy, L. M. (2009). Obtaining Ilyanassa snail embryos. Cold Spring Harbor protocols, 2009(4).More infoThe marine gastropod Ilyanassa obsoleta is a long-standing and very useful model for studies of embryonic development. It is an especially important model for spiralian development, and for studies of asymmetric cell division. The embryos are amenable to classic embryological manipulation techniques as well as a growing number of molecular approaches. Ilyanassa is also an important model for studies of metamorphosis, the ecology of parasitism, the effects of environmental contaminants on morphology and sexual function, and comparative neurobiology. Ilyanassa adults are readily obtainable and easy to keep in the laboratory. Although the normal spawning season for Ilyanassa is during early summer, they can produce high-quality embryos nearly year-round in the laboratory. Snails collected in the late fall, winter, or spring can be induced to deposit zygotes before the natural spawning season by warming them to room temperature, and snails collected before the natural spawning season can be made to postpone zygote deposition until needed (up to at least 6 mo) by maintaining them in tanks in a cold room at 4 degrees C-8 degrees C. This protocol describes how to induce embryo production in Ilyanassa snails, collect the embryos, and rear them to the stage required for study.
- Nagy, L., Nagy, L., Gharbiah, M., Gharbiah, M., Cooley, J., Cooley, J., Leise, E. M., Leise, E. M., Nakamoto, A., Nakamoto, A., Rabinowitz, J. S., Rabinowitz, J. S., Lambert, J. D., Lambert, J. D., Nagy, L. M., & Nagy, L. M. (2009). Pressure injection of Ilyanassa snail embryos. Cold Spring Harbor protocols, 2009(4).More infoThe marine gastropod Ilyanassa obsoleta is a long-standing and very useful model for studies of embryonic development. It is an especially important model for spiralian development, and for studies of asymmetric cell division. The embryos are amenable to classic embryological manipulation techniques, as well as a growing number of molecular approaches. Ilyanassa is also an important model for studies of metamorphosis, the ecology of parasitism, the effects of environmental contaminants on morphology and sexual function, and comparative neurobiology. Intracellular microinjection is an important tool, especially for lineage tracing and perturbations of specific genes by knockdown approaches and synthetic mRNA injections. Two methods for the introduction of lineage tracers into particular cells are routine in Ilyanassa. Iontophoresis of charged molecules, such as fluorophore-dextran conjugates can be accomplished using a simply built current generator. Injection of an oil-based solution containing the fluorescent probe 1,1-dioctadecyl-3,3,3',3'-tetramethyl indocarbocyanine perchlorate (DiI) is also straightforward. However, injection of oil-based solutions and iontophoresis have not been useful for delivering water-soluble reagents to perturb gene function, and pressure injection of aqueous solutions has been more challenging. This protocol describes a recently optimized procedure for the pressure injection of aqueous solutions into Ilyanassa embryos and zygotes with high rates of survival and normal development. The key parameters seem to be the injection needles, injection media, and the stage of injected embryos.
- Nagy, L., Nagy, L., Gharbiah, M., Gharbiah, M., Cooley, J., Cooley, J., Leise, E. M., Leise, E. M., Nakamoto, A., Nakamoto, A., Rabinowitz, J. S., Rabinowitz, J. S., Lambert, J. D., Lambert, J. D., Nagy, L. M., & Nagy, L. M. (2009). The snail Ilyanassa: a reemerging model for studies in development. Cold Spring Harbor protocols, 2009(4).More infoIlyanassa obsoleta is a marine gastropod that is a long-standing and very useful model for studies of embryonic development. It is especially important as a model for the spiralian development program, a distinctive mode of early development shared by a large group of animal phyla, but poorly understood. Ilyanassa adults are readily obtainable and easy to keep in the laboratory, and they produce large numbers of embryos throughout most of the year. The embryos are amenable to classic embryological manipulation techniques as well as a growing number of molecular approaches. In this article, we present an overview of aspects of its biology and use as a model organism.
- Nagy, L., Nagy, L., Sewell, W., Sewell, W., Williams, T., Williams, T., Cooley, J., Cooley, J., Terry, M., Terry, M., Ho, R., Ho, R., Nagy, L. M., & Nagy, L. M. (2008). Evidence for a novel role for dachshund in patterning the proximal arthropod leg. Development genes and evolution, 218(6).More infoThe branchiopod crustacean Triops longicaudatus has paddlelike thoracic appendages with few joints and multiple marginal lobes. Here, we explore the degree to which the Triops limb is patterned by the same network of genes known to pattern the uniramous, multi-jointed insect appendage. Insect leg patterning proceeds through a process of subdividing the leg into proximal, intermediate, and distal regions by the activity of the transcription factors hth/exd, dac, and Dll. The immature Triops limb is subdivided into large, discrete regional domains (proximal and distal) as defined by nuclear-EXD and DLL. We show that HTH expression in Triops overlaps cell-to-cell with n-EXD expression. In addition, dac is expressed in two domains: (1) adjacent to and partially overlapping the distal Dll domain and (2) along the medial margin of the developing leg. The DAC domain adjacent to the distal Dll domain supports the early establishment of the expected intermediate domain of DAC expression. The medial expression domain resolves over time into a series of reiterated stripes located on the lower side of each medial lobe. Later, this expression pattern correlates with the sclerotized regions associated with limb flexion. We propose that these stripes of DAC expression play a role in forming reiterated medial lobes. Unlike Drosophila, where the proximal distal patterning of the leg is coincident with patterning of reiterated structures (segments), we hypothesize that the patterning in Triops may reflect an ancestral state where the patterning of reiterated medial structures was not coincident with proximodistal limb patterning.
- Reed, R. D., McMillan, W. O., & Nagy, L. M. (2008). Gene expression underlying adaptive variation in Heliconius wing patterns: Non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proceedings of the Royal Society B: Biological Sciences, 275(1630), 37-45.More infoPMID: 17956848;PMCID: PMC2562400;Abstract: Geographical variation in the mimetic wing patterns of the butterfly Heliconius erato is a textbook example of adaptive polymorphism; however, little is known about how this variation is controlled developmentally. Using microarrays and qPCR, we identified and compared expression of candidate genes potentially involved with a red/yellow forewing band polymorphism in H. erato. We found that transcripts encoding the pigment synthesis enzymes cinnabar and vermilion showed pattern- and polymorphism-related expression patterns, respectively. cinnabar expression was associated with the forewing band regardless of pigment colour, providing the first gene expression pattern known to be correlated with a major Heliconius colour pattern. In contrast, vermilion expression changed spatially over time in red-banded butterflies, but was not expressed at detectable levels in yellow-banded butterflies, suggesting that regulation of this gene may be involved with the red/yellow polymorphism. Furthermore, we found that the yellow pigment, 3-hydroxykynurenine, is incorporated into wing scales from the haemolymph rather than being synthesized in situ. We propose that some aspects of Heliconius colour patterns are determined by spatio-temporal overlap of pigment gene transcription prepatterns and speculate that evolutionary changes in vermilion regulation may in part underlie an adaptive colour pattern polymorphism. © 2007 The Royal Society.
- Grbic, M., Khila, A., Lee, K., Bjelica, A., Grbic, V., Whistlecraft, J., Verdon, L., Navajas, M., & Nagy, L. (2007). Mity model: Tetranychus urticae, a candidate for chelicerate model organism. BioEssays, 29(5), 489-496.More infoPMID: 17450600;Abstract: Chelicerates (scorpions, horseshoe crabs, spiders, mites and ticks) are the second largest group of arthropods and are of immense importance for fundamental and applied science. They occupy a basal phylogenetic position within the phylum Arthropoda, and are of crucial significance for understanding the evolution of various arthropod lineages. Chelicerates are vectors of human diseases, such as ticks, and major agricultural pests, such as spider mites, thus this group is also of importance for both medicine and agriculture. The developmental genetics of chelicerates is poorly understood and a challenge for the future progress for many aspects of chelicerate biology is the development of a model organism for this group. Toward this end, we are developing a chelicerate genetic model: the two-spotted spider mite Tetranychus urticae. T. urticae has the smallest genome of any arthropod determined so far (75 Mbp, 60% of the size of the Drosophila genome), undergoes rapid development and is easy to maintain in the laboratory. These features make T. urticae a promising reference organism for the economically important, poorly studied and species-rich chelicerate lineage. © 2007 Wiley Periodicals, Inc.
- Moczek, A. P., & Nagy, L. M. (2005). Diverse developmental mechanisms contribute to different levels of diversity in horned beetles. Evolution and Development, 7(3), 175-185.More infoPMID: 15876190;Abstract: An ongoing challenge to evolutionary developmental biology is to understand how developmental evolution on the level of populations and closely related species relates to macroevolutionary transformations and the origin of morphological novelties. Here we explore the developmental basis of beetle horns, a morphological novelty that exhibits remarkable diversity on a variety of levels. In this study, we examined two congeneric Onthophagus species in which males develop into alternative horned and hornless morphs and different sexes express marked sexual dimorphism. In addition, both species differ in the body region (head vs. thorax) that develops the horn. Using a comparative morphological approach we show that prepupal growth of horn primordia during late larval development, as well as reabsorption of horn primordia during the pupal stage, contribute to horn expression in adults. We also show that variable combinations of both mechanisms are employed during development to modify horn expression of different horns in the same individual, the same horn in different sexes, and different horns in different species. We then examine expression patterns of two transcription factors, Distal-less (Dll) and aristaless (al), in the context of prepupal horn growth in alternative male morphs and sexual dimorphisms in the same two species. Expression patterns are qualitatively consistent with the hypothesis that both transcription factors function in the context of horn development similar to their known roles in patterning a wide variety of arthropod appendages. Our results suggest that the origin of morphological novelties, such as beetle horns, rests, at least in part, on the redeployment of already existing developmental mechanisms, such as appendage patterning processes. Our results also suggest, however, that little to no phylogenetic distance is needed for the evolution of very different modifier mechanisms that allow for substantial modulation of trait expression at different time points during development in different species, sexes, or tissue regions of the same individual. We discuss the implications of our results for our understanding of the evolution of horned beetle diversity and the origin and diversification of morphological novelties. © Blackwell Publishing, Inc.
- Reed, R. D., & Nagy, L. M. (2005). Evolutionary redeployment of a biosynthetic module: Expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evolution and Development, 7(4), 301-311.More infoPMID: 15982367;Abstract: Ommochromes are common among insects as visual pigments; however, in some insect lineages ommochromes have evolved novel functions such as integument coloration and tryptophan secretion. One role of ommochromes, as butterfly wing pigments, can apparently be traced to a single origin in the family Nymphalidae. The synthesis and storage of ommochrome pigments is a complex process that requires the concerted activity of multiple enzyme and transporter molecules. To help understand how this subcellular process appeared in a novel context during evolution, we explored aspects of ommochrome pigment development in the wings of the nymphalid butterfly Vanessa cardui. Using chromatography and radiolabeled precursor incorporation studies we identified the ommochrome xanthommatin as a V. cardui wing pigment. We cloned fragments of two ommochrome enzyme genes, vermilion and cinnabar, and an ommochrome precursor transporter gene, white, and found that these genes were transcribed in wing tissue at relatively high levels during wing scale development. Unexpectedly, however, the spatial patterns of transcription were not associated in a simple way with adult pigment patterns. Although our results suggest that the evolution of ommochrome synthesis in butterfly wings likely arose in part through novel regulation of vermilion, cinnabar, and white transcription, they also point to a complex relationship between transcriptional prepatterns and pigment synthesis in V. cardui. © Blackwell Publishing, Inc.
- Jockusch, E. L., Williams, T. A., & Nagy, L. M. (2004). The evolution of patterning of serially homologous appendages in insects. Development Genes and Evolution, 214(7), 324-338.More infoPMID: 15170569;Abstract: Arthropod bodies are formed by a series of appendage-bearing segments, and appendages have diversified both along the body axis within species and between species. Understanding the developmental basis of this variation is essential for addressing questions about the evolutionary diversification of limbs. We examined the development of serially homologous appendages of two insect species, the beetle Tribolium castaneum and the grasshopper Schistocerca americana. Both species retain aspects of ancestral appendage morphology and development that have been lost in Drosophila, including branched mouthparts and direct development of appendages during embryogenesis. We characterized the expression of four genes important in proximodistal axis development of Drosophila appendages: the secreted signaling factors wingless and decapentaplegic, and the homeodomain transcription factors extradenticle and Distal-less. Our comparisons focus on two aspects of appendage morphology: differentiation of the main axis of serial homologues and the appearance of proximal branches (endites) in the mouthparts. Although Distal-less expression is similar in endites and palps of the mouthparts, the expression of other genes in the endites does not conform to their known roles in axial patterning, leading us to reject the hypothesis that branched insect mouthparts develop by reiteration of the limb patterning network. With the exception of decapentaplegic, patterning of the main appendage axis is generally more similar in direct homologues than in serial homologues. Interestingly, however, phylogenetic comparisons suggest that patterning of serial homologues was more similar in ancestral insects, and thus that the observed developmental differences did not cause the evolutionary divergence in morphology among serial homologues. © Springer-Verlag 2004.
- Wandelt, J., & Nagy, L. M. (2004). Left-right asymmetry: More than one way to coil a shell. Current Biology, 14(16), R654-R656.More infoPMID: 15324681;Abstract: Snail shells can be left-handed or right-handed, sometimes within one species. For over a century, it has commonly been assumed that mirror-image shell coiling in snails is correlated with a mirror- image reversal of early spindle orientation and cleavage. The results of an exciting and elegant new study refute this model, showing that right doesn't have to be the mirror image of left.
- Briscoe, A. D., Bernard, G. D., Szeto, A. S., Nagy, L. M., & White, R. H. (2003). Not all butterfly eyes are created equal: Rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui. Journal of Comparative Neurology, 458(4), 334-349.More infoPMID: 12619069;Abstract: Surveys of spectral sensitivities, visual pigment spectra, and opsin gene sequences have indicated that all butterfly eyes contain ultraviolet-, blue-, and green-sensitive rhodopsins. Some species also contain a fourth or fifth type, related in amino acid sequence to green-sensitive insect rhodopsins, but red shifted in absorbance. By combining electron microscopy, epimicrospectrophotometry, and polymerase chain reaction cloning, we found that the compound eye of Vanessa cardui has the typical ultrastructural features of the butterfly retina but contains only the three common insect rhodopsins. We estimated lambda-max values and relative densities of the rhodopsins in the Vanessa retina (0.72, P530; 0.12, P470; and 0.15, P360) from microspectrophotometric measurements and calculations based on a computational model of reflectance spectra. We isolated three opsin-encoding cDNA fragments that were identified with P530, P470, and P360 by homology to the well-characterized insect rhodopsin families. The retinal mosaic was mapped by opsin mRNA in situ hybridization and found to contain three kinds of ommatidia with respect to their patterns of short wavelength rhodopsin expression. In some ommatidia, P360 or P470 was expressed in R1 and R2 opposed receptor cells; in others, one cell expressed P360, whereas its complement expressed P470. P530 was expressed in the other seven cells of all ommatidia. P470-expressing cells were abundant in the ventral retina but nearly absent dorsally. Our results indicated that there are major differences between the color vision systems of nymphalid and papilionid butterflies: the nymphalid Vanessa has a simpler, trichromatic, system than do the tetrachromatic papilionids that have been studied. © 2003 Wiley-Liss, Inc.
- Lambert, J. D., & Nagy, L. M. (2003). The MAPK cascade in equally cleaving spiralian embryos. Developmental Biology, 263(2), 231-241.More infoPMID: 14597198;Abstract: Spiralian development is shared by several protostome phyla and characterized by regularities in early cleavage, fate map, and larva. Experimental evidence from multiple spiralian species implicates cells in the D quadrant lineage as the organizer of future axial development of the embryo. However, the mechanisms by which the D quadrant is specified differ between species with equal and unequal spiral cleavage. Equally cleaving mollusc embryos establish the D quadrant via cell-cell interactions between the micromeres and macromeres at the 24- to 36-cell stage. In unequally cleaving embryos, the D quadrant is established at the 4-cell stage via asymmetries in the first 2 cell divisions. We have begun to explore the molecular mechanisms of D quadrant patterning in spiralians. Previously, we showed that, in the unequally cleaving embryo of the mollusc Ilyanassa obsoleta, the MAPK pathway is activated and functionally required in 3D and also in the micromeres known to require a signal from 3D. Here, we examine the role of MAPK signaling in 4 spiralians with equal cleavage. In 3 equally cleaving molluscs, the chiton Chaetopleura, the limpet Tectura, and the snail Lymnaea, the MAPK pathway is activated in the 3D cell but not in the overlying micromeres. In the equally cleaving embryo of the polychaete annelid Hydroides, MAPK activation was not detected in the 3D macromere but was observed in one of its daughter cells, 4d. In addition, inhibiting Tectura MAPK activation disrupts differentiation of 3D and cells induced by it, supporting a functional role for MAPK in axis specification in equally cleaving spiralians. Thus, MAPK signaling may have a conserved role in the D quadrant organizer cell 3D in molluscs. However, there have been at least 2 evolutionary changes in the activation of the MAPK pathway during spiralian evolution. MAPK function in the Ilyanassa micromeres is a recent cooption and, since the divergence of annelids and molluscs, there has been a shift in onset of MAPK activation between 3D and 4d. We propose that this latter shift correlates with a change in the timing of specification of the secondary embryonic axis. © 2003 Elsevier Inc. All rights reserved.
- Nagy, L., Nagy, L., Lambert, J. D., Lambert, J. D., Nagy, L. M., & Nagy, L. M. (2003). The MAPK cascade in equally cleaving spiralian embryos. Developmental biology, 263(2).More infoSpiralian development is shared by several protostome phyla and characterized by regularities in early cleavage, fate map, and larva. Experimental evidence from multiple spiralian species implicates cells in the D quadrant lineage as the organizer of future axial development of the embryo. However, the mechanisms by which the D quadrant is specified differ between species with equal and unequal spiral cleavage. Equally cleaving mollusc embryos establish the D quadrant via cell-cell interactions between the micromeres and macromeres at the 24- to 36-cell stage. In unequally cleaving embryos, the D quadrant is established at the 4-cell stage via asymmetries in the first 2 cell divisions. We have begun to explore the molecular mechanisms of D quadrant patterning in spiralians. Previously, we showed that, in the unequally cleaving embryo of the mollusc Ilyanassa obsoleta, the MAPK pathway is activated and functionally required in 3D and also in the micromeres known to require a signal from 3D. Here, we examine the role of MAPK signaling in 4 spiralians with equal cleavage. In 3 equally cleaving molluscs, the chiton Chaetopleura, the limpet Tectura, and the snail Lymnaea, the MAPK pathway is activated in the 3D cell but not in the overlying micromeres. In the equally cleaving embryo of the polychaete annelid Hydroides, MAPK activation was not detected in the 3D macromere but was observed in one of its daughter cells, 4d. In addition, inhibiting Tectura MAPK activation disrupts differentiation of 3D and cells induced by it, supporting a functional role for MAPK in axis specification in equally cleaving spiralians. Thus, MAPK signaling may have a conserved role in the D quadrant organizer cell 3D in molluscs. However, there have been at least 2 evolutionary changes in the activation of the MAPK pathway during spiralian evolution. MAPK function in the Ilyanassa micromeres is a recent cooption and, since the divergence of annelids and molluscs, there has been a shift in onset of MAPK activation between 3D and 4d. We propose that this latter shift correlates with a change in the timing of specification of the secondary embryonic axis.
- Lambert, J. D., & Nagy, L. M. (2002). Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature, 420(6916), 682-686.More infoPMID: 12478296;Abstract: During development, different cell fates are generated by cell-cell interactions or by the asymmetric distribution of patterning molecules. Asymmetric inheritance is known to occur either through directed transport along actin microfilaments into one daughter cell1,2 or through capture of determinants by a region of the cortex inherited by one daughter3-5. Here we report a third mechanism of asymmetric inheritance in a mollusc embryo. Different messenger RNAs associate with centrosomes in different cells αnd are subsequently distributed asymmetrically during division. The segregated mRNAs are diffusely distributed in the cytoplasm and then localize, in a microtubule-dependent manner, to the pericentriolar matrix. During division, they dissociate from the core mitotic centrosome and move by means of actin filaments to the presumptive animal daughter cell cortex. In experimental cells with two interphase centrosomes, mRNAs accumulate on the correct centrosome, indicating that differences between centrosomes control mRNA targeting. Blocking the accumulation of mRNAs on the centrosome shows that this event is required for subsequent cortical localization. These events produce a complex pattern of mRNA localization, in which different messages distinguish groups of cells with the same birth order rank and similar developmental potentials.
- Nagy, L., Nagy, L., Lambert, J. D., Lambert, J. D., Nagy, L. M., & Nagy, L. M. (2002). Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature, 420(6916).More infoDuring development, different cell fates are generated by cell-cell interactions or by the asymmetric distribution of patterning molecules. Asymmetric inheritance is known to occur either through directed transport along actin microfilaments into one daughter cell or through capture of determinants by a region of the cortex inherited by one daughter. Here we report a third mechanism of asymmetric inheritance in a mollusc embryo. Different messenger RNAs associate with centrosomes in different cells and are subsequently distributed asymmetrically during division. The segregated mRNAs are diffusely distributed in the cytoplasm and then localize, in a microtubule-dependent manner, to the pericentriolar matrix. During division, they dissociate from the core mitotic centrosome and move by means of actin filaments to the presumptive animal daughter cell cortex. In experimental cells with two interphase centrosomes, mRNAs accumulate on the correct centrosome, indicating that differences between centrosomes control mRNA targeting. Blocking the accumulation of mRNAs on the centrosome shows that this event is required for subsequent cortical localization. These events produce a complex pattern of mRNA localization, in which different messages distinguish groups of cells with the same birth order rank and similar developmental potentials.
- Williams, T. A., Nulsen, C., & Nagy, L. M. (2002). A complex role for Distal-less in crustacean appendage development. Developmental Biology, 241(2), 302-312.More infoPMID: 11784113;Abstract: The developing leg of Drosophila is initially patterned by subdivision of the leg into proximal and distal domains by the activity of the homeodomain proteins Extradenticle (Exd) and Distal-less (Dll). These early domains of gene expression are postulated to reflect a scenario of limb evolution in which an undifferentiated appendage outgrowth was subdivided into two functional parts, the coxapodite and telopodite. The legs of most arthropods have a more complex morphology than the simple rod-shaped leg of Drosophila. We document the expression of Dll and Exd in two crustacean species with complex branched limbs. We show that in these highly modified limbs there is a Dll domain exclusive of Exd but there is also extensive overlap in Exd and Dll expression. While arthropod limbs all appear to have distinct proximal and distal domains, those domains do not define homologous structures throughout arthropods. In addition, we find a striking correlation throughout the proximal/distal extent of the leg between setal-forming cells and Dll expression. We postulate that this may reflect a pleisiomorphic function of Dll in development of the peripheral nervous system. In addition, our results confirm previous observations that branch formation in multiramous arthropod limbs is not regulated by a simple iteration of the proximal/distal patterning module employed in Drosophila limb development. © 2001 Elsevier Science.
- Lambert, J. D., & Nagy, L. M. (2001). MAPK signaling by the D quadrant embryonic organizer of the mollusc llyanassa obsoleta. Development, 128(1), 45-56.More infoPMID: 11092810;Abstract: Classical experiments performed on the embryo of the mollusc Ilyanassa obsoleta demonstrate that the 3D macromere acts as an embryonic organizer, by signaling to other cells and inducing them to assume the correct pattern of cell fates. We have discovered that MAP kinase signaling is activated in the cells that require the signal from 3D for normal differentiation. Preventing specification of the D quadrant lineage by removing the polar lobe disrupts the pattern of MAPK activation, as does ablation of the 3D macromere itself. Blocking MAPK activation with the MAP Kinase inhibitor U0126 produces larvae that differentiate the same limited complement of tissues as D quadrant deletions. Our results suggest that the MAP Kinase signaling cascade transduces the inductive signal from 3D and specifies cell fate among the cells that receive the signal.
- Popadić, A., & Nagy, L. (2001). Conservation and variation in Ubx expression among chelicerates. Evolution and Development, 3(6), 391-396.More infoPMID: 11806634;Abstract: Chelicerates are an ancient arthropod group with a distinct body plan composed of an anterior (prosoma) and a posterior portion (opisthosoma). The expression of the Hox gene Ultrabithorax (Ubx) has been examined in a single representative of the chelicerates, the spider Cupiennius salei. In spiders, Ubx expression starts in the second opisthosomal segment (O2). Because the first opisthosomal segment (O1) in spiders is greatly reduced relative to other chelicerates, we hypothesized that the observed Ubx expression pattern might be secondarily modified. Shifts in the anterior boundary of the expression of Ubx have been correlated with functional shifts in morphology within malacostracan crustaceans. Thus, the boundary of Ubx expression between chelicerates with different morphologies in their anterior opisthosoma could also be variable. To test this prediction, we examined the expression patterns of Ubx and abdominal-A (collectively referred to as UbdA) in two basal chelicerate lineages, scorpions and xiphosurans (horseshoe crabs), which exhibit variation in the morphology of their anterior opisthosoma. In the scorpion Paruroctonus mesaensis, the anterior border of early expression of UbdA is in a few cells in the medial, posterior region of the O2 segment, with a predominant expression in O3 and posterior. Expression later spreads to encompass the whole O2 segment and a ventral, posterior portion of the O1 segment. In the xiphosuran Limulus polyphemus, early expression of UbdA has an anterior boundary in the segment. Later in development, the anterior boundary moves forward one segment to the chilarial (O1) segment. Thus, the earliest expression boundary of UbdA lies within the second opisthosomal segment in all the chelicerates examined. These results suggest that rather than being derived, the spider UbdA expression in O2 likely reflects the ancestral expression boundary. Changes in the morphology of the first opisthosomal segment are either not associated with changes in UbdA expression or correlate with late developmental changes in UbdA expression.
- Williams, T. A., & Nagy, L. M. (2001). Developmental Modularity and the Evolutionary Diversification of Arthropod Limbs. Journal of Experimental Zoology, 291(3), 241-257.More infoPMID: 11598913;Abstract: Segmentation is one of the most salient characteristics of arthropods, and differentiation of segments along the body axis is the basis of arthropod diversification. This article evaluates whether the evolution of segmentation involves the differentiation of already independent units, i.e., do segments evolve as modules? Because arthropod segmental differentiation is commonly equated with differential character of appendages, we analyze appendages by comparing similarities and differences in their development. The comparison of arthropod limbs, even between species, is a comparison of serially repeated structures. Arthropod limbs are not only reiterated along the body axis, but limbs themselves can be viewed as being composed of reiterated parts. The interpretation of such reiterated structures from an evolutionary viewpoint is far from obvious. One common view is that serial repetition is evidence of a modular organization, i.e., repeated structures with a common fundamental identity that develop semi-autonomously and are free to diversify independently. In this article, we evaluate arthropod limbs from a developmental perspective and ask: are all arthropod limbs patterned using a similar set of mechanisms which would reflect that they all share a generic coordinate patterning system? Using Drosophila as a basis for comparison, we find that appendage primordia, positioned along the body using segmental patterning coordinates, do indeed have elements of common identity. However, we do not find evidence of a single coordinate system shared either between limbs or among limb branches. Data concerning the other diagnostic of developmental modularity - semi-autonomy of development - are not currently available for sufficient taxa. Nonetheless, some data comparing patterns of morphogenesis provide evidence that limbs cannot always be temporally or spatially decoupled from the development of their neighbors, suggesting that segment modularity is a derived character. © 2001 Wiley-Liss, Inc.
- Jockusch, E. L., Nulsen, C., Newfeld, S. J., & Nagy, L. M. (2000). Leg development in flies versus grasshoppers: Differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway. Development, 127(8), 1617-1626.More infoPMID: 10725238;Abstract: All insect legs are structurally similar, characterized by five primary segments. However, this final form is achieved in different ways. Primitively, the legs developed as direct outgrowths of the body wall, a condition retained in most insect species. In some groups, including the lineage containing the genus Drosophila, legs develop indirectly from imaginal discs. Our understanding of the molecular mechanisms regulating leg development is based largely on analysis of this derived mode of leg development in the species D. melanogaster. The current model for Drosophila leg development is divided into two phases, embryonic allocation and imaginal disc patterning, which are distinguished by interactions among the genes wingless (wg), decapentaplegic (dpp) and distalless (dll). In the allocation phase, dll is activated by wg but repressed by dpp. During imaginal disc patterning, dpp and wg cooperatively activate dll and also indirectly inhibit the nuclear localization of Extradenticle (Exd), which divide the leg into distal and proximal domains. In the grasshopper Schistocerca americana, the early expression pattern of dpp differs radically from the Drosophila pattern, suggesting that the genetic interactions that allocate the leg differ between the two species. Despite early differences in dpp expression, wg, D11 and Exd are expressed in similar patterns throughout the development of grasshopper and fly legs, suggesting that some aspects of proximodistal (P/D) patterning are evolutionarily conserved. We also detect differences in later dpp expression, which suggests that dpp likely plays a role in limb segmentation in Schistocerca, but not in Drosophila. The divergence in dpp expression is surprising given that all other comparative data on gene expression during insect leg development indicate that the molecular pathways regulating this process are conserved. However, it is consistent with the early divergence in developmental mode between fly and grasshopper limbs.
- Nulsen, C., & Nagy, L. M. (1999). The role of wingless in the development of multibranched crustacean limbs. Development Genes and Evolution, 209(6), 340-348.More infoPMID: 10370115;Abstract: Arthropods are the most diverse and speciose group of organisms on earth. A key feature in their successful radiation is the ease with which various appendages become readily adapted to new functions in novel environments. Arthropod limbs differ radically in form and function, from unbranched walking legs to multibranched swimming paddles. To uncover the developmental and genetic mechanisms underlying this diversification in form, we ask whether a three-signal model of limb growth based on Drosophila experiments is used in the development of arthropod limbs with variant shape. We cloned a Wnt-1 ortholog (Tlwnt-1) from Triops longicaudatus, a basal crustacean with a multibranched limb. We examined the mRNA in situ hybridization pattern during larval development to determine whether changes in wg expression are correlated with innovation in limb form. During larval growth and segmentation Tlwnt-1 is expressed in a segmentally reiterated pattern in the trunk. Unexpectedly, this pattern is restricted to the ventral portion of the epidermis. During early limb formation the single continuous stripe of Tlwnt-1 expression in each segment becomes ventrolaterally restricted into a series of shorter stripes. Some but not all of these shorter stripes correspond to what becomes the ventral side of a developing limb branch. We conclude that the Drosophila model of limb development cannot explain all types of arthropod proximodistal outgrowths, and that the multibranched limb of Triops develops from an early reorganization of the ventral body wall. In Triops, Tlwnt-1 plays a semiconservative role similar to that played by Drosophila wingless in segmentation and limb formation, and morphological innovation in limb form arises in part through an early modulation in the expression of the Tlwnt-1 gene.
- Grbić, M., Nagy, L. M., & Strand, M. R. (1998). Development of polyembryonic insects: A major departure from typical insect embryogenesis. Development Genes and Evolution, 208(2), 69-81.More infoPMID: 9569348;Abstract: The parasitic wasp Copidosoma floridanum represents the most extreme form of polyembryonic development known, forming up to 2000 embryos from a single egg. To understand the mechanisms of embryonic patterning in polyembryonic wasps and the evolutionary changes that led to this form of development we have analyzed embryonic development at the cellular level using confocal and scanning electron microscopy. C. floridanum embryogenesis can be divided into three phases: (1) early cleavage that leads to formation of a primary morula, (2) a proliferative phase that involves partitioning of embryonic cells into thousands of morulae, and (3) morphogenesis whereby individual embryos develop into larvae. This developmental program represents a major departure from typical insect embryogenesis, and we describe several features of morphogenesis unusual for insects. The early development of polyembryonic wasps, which likely evolved in association with a shift in life history to endoparasitism, shows several analogies with mammalian embryogenesis, including early separation of extraembryonic and embryonic cell lineages, formation of a morula and embryonic compaction. However, the late morphogenesis of polyembryonic wasps proceeds in a fashion conserved in all insects. Collectively, this suggests a lack of developmental constraints in early development, but a strong conservation of the phylotypic stage.
- Nagy, L. (1998). Changing patterns of gene regulation in the evolution of arthropod morphology. American Zoologist, 38(6), 818-828.More infoAbstract: SYNOPSIS. What can the comparative study of gene expression patterns during development contribute to the study of phylogeny? I discuss the basic properties of gene networks that function in development, using information gleaned from developmental model systems. Using examples from the analysis of anteroposterior, dorsoventral and proximodistal axis formation, I outline how the gene networks that pattern these three axes of development are linked in evolution. Finally, I discuss the types of analyses necessary to further our understanding of how gene networks function in regulating the evolution of morphology.
- Jockusch, E. L., & Nagy, L. M. (1997). Insect evolution: How did insect wings originate?. Current Biology, 7(6), R358-R361.More infoPMID: 9197228;Abstract: Recent developmental studies aimed at elucidating the evolutionary origin of insect wings highlight the difficulties of identifying homology between dramatically different structures.
- Grbic, M., Nagy, L. M., & Strand, M. (1996). Pattern duplications in larvae of the polyembryonic wasp Copidosoma floridanum. Development Genes and Evolution, 206(4), 281-287.More infoPMID: 24173567;Abstract: Copidosoma floridanum is a polyembryonic wasp that undergoes total cleavage of the egg followed by proliferation of blastomeres to produce up to 2,000 embryos from a single egg. This unusual mode of development raises several questions about how axial polarity is established in individual embryonic primordia. By examining embryonic development of larvae with duplicated structures (conjoined larvae), we determined that conjoined larvae form by mislocalization of two embryonic primordia to a common chamber of the extraembryonic membrane that surrounds individual embryos. Analysis of an anterior marker, Distalless, in mislocalized early embryos indicated that anterior structures form independently of one another. This suggests each embryonic primordium has some intrinsic polarity. However, during germband extension embryos usually fuse in register with each other, resulting in conjoined larvae with heads facing each other. Analysis of the posterior segmental marker, Engrailed, in conjoined embryos suggested that fusion in register initiates during, germband extension. Thus, even though embryonic primordia initially have a random axial orientation, conjoined larvae usually possess a common orientation due to reorientation during germband extension. These observations suggest that differential cellular affinities during segmentation play an important role in embryo fusion.
- Grbic, M., Nagy, L. M., & Strand, M. (1996). Pattern duplications in larvae of the polyembryonic wasp Copidosoma floridanum. Roux's Archives of Developmental Biology, 206(4), 281-287.More infoAbstract: Copidosoma floridanum is a polyembryonic wasp that undergoes total cleavage of the egg followed by proliferation of blastomeres to produce up to 2,000 embryos from a single egg. This unusual mode of development raises several questions about how axial polarity is established in individual embryonic primordia. By examining embryonic development of larvae with duplicated structures (conjoined larvae), we determined that conjoined larvae form by mislocalization of two embryonic primordia to a common chamber of the extraembryonic membrane that surrounds individual embryos. Analysis of an anterior marker, Distalless, in mislocalized early embryos indicated that anterior structures form independently of one another. This suggests each embryonic primordium has some intrinsic polarity. However, during germband extension embryos usually fuse in register with each other, resulting in conjoined larvae with heads facing each other. Analysis of the posterior segmental marker, Engrailed, in conjoined embryos suggested that fusion in register initiates during germband extension. Thus, even though embryonic primordia initially have a random axial orientation, conjoined larvae usually possess a common orientation due to reorientation during germband extension. These observations suggest that differential cellular affinities during segmentation play an important role in embryo fusion. © Springer-Verlag 1996.
- Grbić, M., Nagy, L. M., Carroll, S. B., & Strand, M. (1996). Polyembryonic development: Insect pattern formation in a cellularized environment. Development, 122(3), 795-804.More infoPMID: 8631257;Abstract: The polyembryonic wasp Copidosoma floridanum produces up to 2000 individuals from a single egg. During the production of individual embryos the original anteroposterior axis of the egg is lost and axial patterning must subsequently be reestablished within each embryo. The mechanism by which this occurs is unknown. In most insects, egg polarity is established during oogenesis and early development takes place in a syncytium. In Drosophila melanogaster, the syncytium is considered essential for establishing the morphogenetic gradients that initiate segmental patterning. However, we found that development of C. floridanum occurs almost exclusively in a cellularized environment. To determine whether the D. melanogaster patterning cascade is conserved in the absence of a syncytium, we analyzed the expression of Even-skipped, Engrailed and Ultrabithorax/Abdominal-A during polyembryonic development. Here we show that in spite of the absence of a syncytium, the elements of the D. melanogaster segmentation hierarchy are conserved. The segment-polarity gene Engrailed and the homeotic genes Ultrabithorax/Abdominal-A are expressed in a conserved pattern relative to D. melanogaster. However, we detect an alteration in the expression of the Even-skipped antigen. Even-skipped is initially expressed in segmentally reiterated stripes and not in a pair-rule pattern as it is in D. melanogaster. We also observe that the expression of these regulatory proteins does not occur during the early proliferative phases of polyembryony. Our results indicate that a syncytium is not required for segmental patterning in this insect.
- Williams, T. A., & Nagy, L. M. (1996). Comparative limb development in insects and crustaceans. Seminars in Cell and Developmental Biology, 7(4), 615-628.More infoAbstract: Developmental genetics has revealed several molecular players critical for patterning the adult leg in Drosophila. Comparisons throughout insects and crustaceans reveal that some of the molecular mechanisms that initiate limb patterning are conserved: limbs seem to always consist of anterior/posterior compartments, and their initial proximal/distal outgrowth is marked by Distalless expression. It remains unknown whether the developmental mechanisms that subsequently generate differences in limb morphology are themselves diverse. A comparative perspective suggests that one important evolutionary transition in limb development was the evolution of joints and limb segmentation. ©1996 Academic Press Ltd.
- Panganiban, G., Sebring, A., Nagy, L., & Carroll, S. (1995). The development of crustacean limbs and the evolution of arthropods. Science, 270(5240), 1363-1366.More infoPMID: 7481825;Abstract: Arthropods exhibit great diversity in the position, number, morphology, and function of their limbs. The evolutionary relations among limb types and among the arthropod groups that bear them (insects, crustaceans, myriapods, and chelicerates) are controversial. Here, the use of molecular probes, including an antibody to proteins encoded by arthropod and vertebrate Distal-less (Dll and Dlx) genes, provided evidence that common genetic mechanisms underlie the development of all arthropod limbs and their branches and that all arthropods derive from a common ancestor. However, differences between crustacean and insect body plans were found to correlate with differences in the deployment of particular homeotic genes and in the ways that these genes regulate limb development.
- Williams, T. A., & Nagy, L. M. (1995). Brine shrimp add salt to the stew. Current Biology, 5(12), 1330-1333.More infoPMID: 8749376;Abstract: The expression patterns of homeotic genes in a crustacean - the brine shrimp Artemia franciscana - provide a new perspective on the evolution of arthropod body plans.
- Nagy, L. M. (1994). A glance posterior. Current Biology, 4(9), 811-814.More infoPMID: 7865024;Abstract: Segmentation gene expression patterns can be radically different in some short-germ and long-germ insects, but other types of short/intermediate-germ insects may use Drosophila-like segmentation mechanisms.
- Nagy, L. M., & Carroll, S. (1994). Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature, 367(6462), 460-463.More infoPMID: 8107804;Abstract: During embryogenesis, all insects reach a conserved, or phylotypic, stage at which all future segments are present. Different insects, however, arrive at this stage by overtly different pathways. In the long-germ insect Drosophila melanogaster, segmentation of the entire embryo occurs nearly simultaneously and results from the action of a cascade of transcriptional regulatory factors that operate in the acellular environment of the syncytial blastoderm. In short-germ insects, segmentation occurs in an anterior-to-posterior sequence, within a cellular environment, and might then be dependent on intercellular signalling. To compare the molecular mechanisms of segmentation, we have isolated a homologue of the Drosophila wingless gene, a mediator of cell-cell communications, from the short-germ beetle Tribolium castaneum. The principal features of wingless expression patterns in Drosophila are conserved in Tribolium, including its early deployment in rostral and caudal domains in the blastoderm, its segmental iteration in cells immediately anterior to cells expressing the engrailed gene, and its later restriction to a ventral sector of the developing appendages.
- Nagy, L., Riddiford, L., & Kiguchi, K. (1994). Morphogenesis in the early embryo of the lepidopteran Bombyx mori. Developmental Biology, 165(1), 137-151.More infoPMID: 8088432;Abstract: The regional patterns of nuclear and cell division and the changes in size and shape of the developing Bombyx mori embryo were monitored from just prior to blastoderm formation until the onset of gastrulation. Nuclear invasion of the periphery and subsequent cellularization occurs with a marked anterior to posterior gradient. Consequently, there is no syncytial blastoderm stage in which all nuclei simultaneously rest at the periphery. In addition, the posteriormost blastoderm cells do not form pole cells. Prior to gastrulation, the Bombyx blastoderm cells undergo several unusual types of cell behaviors, indicated in part by the modifications and specializations of their lateral edges. Subsequent to the completion of cellularization, localized regions of mitosis can be found within the germ anlage, but at the stage monitored, just prior to the onset of gastrulation, these regions do not appear to be the equivalent of the Drosophila mitotic domains. The implications of these findings for modeling how segmental fates are established in insects are discussed. This work confirms and extends the work of earlier histological investigations of Bombyx development.
- Panganiban, G., Nagy, L., & Carroll, S. B. (1994). The role of the Distal-less gene in the development and evolution of insect limbs. Current Biology, 4(8), 671-675.More infoPMID: 7953552;Abstract: Background: Arthropod diversity is apparent in the variations in limb number, type, and position along the body axis. Among the insects, for example, butterflies and moths (Lepidoptera) develop larval abdominal and caudal appendages ('prolegs'), whereas flies (Diptera) do not. Comparative studies of the expression and regulation during development of limb-patterning genes, such as Distal-less (Dll), may provide insights into arthropod evolution. Results: We report the cloning of a Dll homolog from the butterfly Precis coenia, and present data showing that it is expressed in all developing limbs (except the mandible), including the prolegs; the relationship between Dll and wingless expression observed in Drosophila is conserved in Precis among all limbs. However, Dll is deployed in distinct spatial and temporal patterns within each limb type. Conclusions: These data suggest that Dll function, suppressed in the abdomen early in insect evolution, has been derepressed in Lepidoptera, and also suggest that there is a common mechanism underlying the formation of all insect appendages. The limb-type-specific patterns of Dll expression (and its exclusion from the mandible) indicate that regulation of Dll expression may be critical to limb morphology, and are inconsistent with Dll functioning in a simple distal-to-proximal concentration gradient.
- Warren, R. W., Nagy, L., Selegue, J., Gates, J., & Carroll, S. (1994). Evolution of homeotic gene regulation and function in flies and butterflies. Nature, 372(6505), 458-461.More infoPMID: 7840822;Abstract: IT has been proposed that the evolution of homeotic genes parallels, and to some degree directs, the evolution of segment diversity in the myriapod-insect lineage1-3. But the discovery of discrete Antennapedia complex (ANT-C) and bithorax complex (BX-C) gene members in crustacea4, chelicerates5, annelids6-8 and various insects9-11,as well as in vertebrates12, indicates that the expansion and diversification of homeotic genes preceded the diversification of arthropods and insects. How, then, have these genes influenced the evolution of body plans? To address this question, we now examine homeotic gene expression and regulation in butterflies (Lepidoptera), which, unlike flies, possess larval abdominal limbs and two pairs of wings. We show that the difference in larval limb number between these insects results from striking changes in BX-C gene regulation in the butterfly abdomen, and we deduce that the wing-patterning genes regulated by Ultrabithorax have diverged in the course of butterfly and fly evolution. These findings have general implications for the role of homeotic genes in animal evolution.
- Nagy, L. M., Booker, R., & Riddiford, L. M. (1991). Isolation and embryonic expression of an abdominal-A-like gene from the lepidopteran, Manduca sexta. Development, 112(1), 119-129.More infoPMID: 1685112;Abstract: Using sequence homology to the Drosophila Antennapedia gene, we isolated a homeobox-containing gene from the lepidopteran, Manduca sexta. Sequence analysis and in situ hybridizations to tissue sections suggest that the Manduca gene encodes a lepidopteran homologue of the Drosophila Bithorax complex gene abdominal-A. The predicted amino acid sequence of a 76 amino acid region that includes the homeobox and the regions immediately flanking it are identical between the Manduca and Drosophila genes. Northern blots reveal that the Manduca abd-A gene is expressed first in the early embryo and continues to be expressed throughout later embryonic and larval stages. In situ hybridizations show that the posterior half of the first abdominal segment marks the anterior border of the Manduca abd-A expression. This expression pattern demonstrates the conservation of parasegments as domains of gene activity in the lepidopteran embryo. The Manduca abd-A expression extends from the posterior half of the first abdominal segment through the tenth abdominal segment, a domain that is greater than that of the Drosophila abd-A expression, and reflects the difference in visible segment number between the two insects.
- Nagy, L. M. (2014, January). Cellular mechanisms underlying posterior segmentation in Tribolium. SICB,.
- Nagy, L. M. (2014, July). Tribolium segmentation: what’s going on in the posterior growth zone.. SDB, Seattle WA,.