Guilherme Gainett, Benjamin C. Klementz, Emily V. W. Setton, Catalina Simian, Hernán A. Iuri, Gregory D. Edgecombe, Alfredo V. Peretti, Prashant P. Sharma
{"title":"A plurality of morphological characters need not equate with phylogenetic accuracy: A rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata","authors":"Guilherme Gainett, Benjamin C. Klementz, Emily V. W. Setton, Catalina Simian, Hernán A. Iuri, Gregory D. Edgecombe, Alfredo V. Peretti, Prashant P. Sharma","doi":"10.1111/ede.12467","DOIUrl":"10.1111/ede.12467","url":null,"abstract":"<p>Recent advances in higher-level invertebrate phylogeny have leveraged shared features of genomic architecture to resolve contentious nodes across the tree of life. Yet, the interordinal relationships within Chelicerata have remained recalcitrant given competing topologies in recent molecular analyses. As such, relationships between topologically unstable orders remain supported primarily by morphological cladistic analyses. Solifugae, one such unstable chelicerate order, has long been thought to be the sister group of Pseudoscorpiones, forming the clade Haplocnemata, on the basis of eight putative morphological synapomorphies. The discovery, however, of a shared whole genome duplication placing Pseudoscorpiones in Arachnopulmonata provides the opportunity for a simple litmus test evaluating the validity of Haplocnemata. Here, we present the first developmental transcriptome of a solifuge (<i>Titanopuga salinarum</i>) and survey copy numbers of the homeobox genes for evidence of systemic duplication. We find that over 70% of the identified homeobox genes in <i>T. salinarum</i> are retained in a single copy, while representatives of the arachnopulmonates retain orthologs of those genes as two or more copies. Our results refute the placement of Solifugae in Haplocnemata. Subsequent reevaluation of putative interordinal morphological synapomorphies among chelicerates reveals a high incidence of homoplasy, reversals, and inaccurate coding within Haplocnemata and other small clades, as well as Arachnida more broadly, suggesting existing morphological character matrices are insufficient to resolve chelicerate phylogeny.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 4","pages":""},"PeriodicalIF":2.6,"publicationDate":"2023-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12467","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138826788","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"A description of the bat star nervous system throughout larval ontogeny","authors":"Veronica Pagowski","doi":"10.1111/ede.12468","DOIUrl":"10.1111/ede.12468","url":null,"abstract":"<p>Larvae represent a distinct life history stage in which animal morphology and behavior contrast strongly to adult organisms. This life history stage is a ubiquitous aspect of animal life cycles, particularly in the marine environment. In many species, the structure and function of the nervous system differ significantly between metamorphosed juveniles and larvae. However, the distribution and diversity of neural cell types in larval nervous systems remains incompletely known. Here, the expression of neurotransmitter and neuropeptide synthesis and transport genes in the bat star <i>Patiria miniata</i> is examined throughout larval development. This characterization of nervous system structure reveals three main neural regions with distinct but overlapping territories. These regions include a densely innervated anterior region, an enteric neural plexus, and neurons associated with the ciliary band. In the ciliary band, cholinergic cells are pervasive while dopaminergic, noradrenergic, and GABAergic cells show regional differences in their localization patterns. Furthermore, the distribution of some neural subtypes changes throughout larval development, suggesting that changes in nervous system structure align with shifting ecological priorities during different larval stages, before the development of the adult nervous system. While past work has described aspects of <i>P. miniata</i> larval nervous system structure, largely focusing on early developmental timepoints, this work provides a comprehensive description of neural cell type localization throughout the extensive larval period.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138715523","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The interglenoid tubercle of the atlas is ancestral to lissamphibians","authors":"Dana E. Korneisel, Sara Hassan, Hillary C. Maddin","doi":"10.1111/ede.12466","DOIUrl":"10.1111/ede.12466","url":null,"abstract":"<p>Lissamphibians, represented today by frogs, salamanders, and caecilians, diverged deep in the tetrapod tree of life. Extensive morphological adaptations to disparate lifestyles have made linking extant lissamphibians to one another and to their extinct relatives difficult and controversial. However, the discovery of a feature on the atlas of the frog <i>Xenopus laevis</i>, may add to the small set of osteological traits that unite lissamphibians. In this study, we combine our observations of atlas development in <i>X. laevis</i> with a deep examination of atlantal interglenoid tubercle (TI) occurrence in fossil taxa. The TI is shown herein to occur transiently on the ossifying atlas of roughly one-third of <i>X. laevis</i> tadpoles but is absent in adults of this species. In ancestral character state estimations (ACSE), within the evolutionary context of lissamphibians as dissorophoid temnospondyls, this feature is found to be ancestrally shared among lissamphibians, its presence is uncertain in stem batrachians, and then the TI is lost in extant caecilians and frogs. However, our data suggests apparent TI loss around the origin of frogs may be explained by its ontogenetically transient nature. The only nonamphibian tetrapods with a TI are “microsaurs,” and this similarity is interpreted as one of many convergences that resulted from convergent evolutionary processes that occurred in the evolution of “microsaurs” and lissamphibians. The TI is thus interpreted to be ancestral to lissamphibians as it is found to be present in some form throughout each extant lissamphibian clade's history.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-12-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12466","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138693325","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Utilizing geometric morphometrics to investigate gene function during organ growth: Insights through the study of beetle horn shape allometry","authors":"Patrick T. Rohner, Yonggang Hu, Armin P. Moczek","doi":"10.1111/ede.12464","DOIUrl":"10.1111/ede.12464","url":null,"abstract":"<p>Static allometry is a major component of morphological variation. Much of the literature on the development of allometry investigates how functional perturbations of diverse pathways affect the relationship between trait size and body size. Often, this is done with the explicit objective to identify developmental mechanisms that enable the sensing of organ size and the regulation of relative growth. However, changes in relative trait size can also be brought about by a range of other distinctly different developmental processes, such as changes in patterning or tissue folding, yet standard univariate biometric approaches are usually unable to distinguish among alternative explanations. Here, we utilize geometric morphometrics to investigate the degree to which functional genetic manipulations known to affect the <i>size</i> of dung beetle horns also recapitulate the effect of horn <i>shape</i> allometry. We reasoned that the knockdown phenotypes of pathways governing relative growth should closely resemble shape variation induced by natural allometric variation. In contrast, we predicted that if genes primarily affect alternative developmental processes, knockdown effects should align poorly with shape allometry. We find that the knockdown effects of several genes (e.g., <i>doublesex, Foxo</i>) indeed closely aligned with shape allometry, indicating that their corresponding pathways may indeed function primarily in the regulation of relative trait growth. In contrast, other knockdown effects (e.g., <i>Distal-less</i>, <i>dachs</i>) failed to align with allometry, implicating these pathways in potentially scaling-independent processes. Our findings moderate the interpretation of studies focusing on trait length and highlight the usefulness of multivariate approaches to study allometry and phenotypic plasticity.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12464","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138470143","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lucia Irazábal-González, Daniel S. Wright, Martine E. Maan
{"title":"Developmental and environmental plasticity in opsin gene expression in Lake Victoria cichlid fish","authors":"Lucia Irazábal-González, Daniel S. Wright, Martine E. Maan","doi":"10.1111/ede.12465","DOIUrl":"10.1111/ede.12465","url":null,"abstract":"<p>In many organisms, sensory abilities develop and evolve according to the changing demands of navigating, foraging, and communication across different environments and life stages. Teleost fish inhabit heterogeneous light environments and exhibit a large diversity in visual system properties among species. Cichlids are a classic example of this diversity; visual system variation is generated by different tuning mechanisms that involve both genetic factors and phenotypic plasticity. Here, we document the developmental progression of visual pigment gene expression in Lake Victoria cichlids and test if these patterns are influenced by variation in light conditions. We reared two sister species of <i>Pundamilia</i> to adulthood in two distinct visual conditions that resemble the light environments that they naturally inhabit in Lake Victoria. We also included interspecific first-generation hybrids. We focused on the four opsins that are expressed in <i>Pundamilia</i> adults (using real-time quantitative polymerase chain reaction (RT-qPCR)) (<i>SWS2B</i>, <i>SWS2A</i>, <i>RH2A</i>, and <i>LWS</i>) at 17 time points. We find that opsin expression profiles progress from shorter-wavelength sensitive opsins to longer-wavelength sensitive opsins with increasing age, in both species and their hybrids. The developmental trajectories of opsin expression also responded plastically to the visual conditions. Developmental and environmental plasticity in opsin expression may provide an important stepping stone in the evolution of cichlid visual system diversity.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12465","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138470142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Got milkweed? Genetic assimilation as potential source for the evolution of nonmigratory monarch butterfly wing shape","authors":"Kyra J. A. Nixon, Harald F. Parzer","doi":"10.1111/ede.12463","DOIUrl":"10.1111/ede.12463","url":null,"abstract":"<p>Monarch butterflies (<i>Danaus plexippus</i>) are well studied for their annual long-distance migration from as far north as Canada to their overwintering grounds in Central Mexico. At the end of the cold season, monarchs start to repopulate North America through short-distance migration over the course of multiple generations. Interestingly, some populations in various tropical and subtropical islands do not migrate and exhibit heritable differences in wing shape and size, most likely an adaptation to island life. Less is known about forewing differences between long- and short-distance migrants in relation to island populations. Given their different migratory behaviors, we hypothesized that these differences would be reflected in wing morphology. To test this, we analyzed forewing shape and size of three different groups: nonmigratory, lesser migratory (migrate short-distances), and migratory (migrate long-distances) individuals. Significant differences in shape appear in all groups using geometric morphometrics. As variation found between migratory and lesser migrants has been shown to be caused by phenotypic plasticity, and lesser migrants develop intermediate forewing shapes between migratory and nonmigratory individuals, we suggest that genetic assimilation might be an important mechanism to explain the heritable variation found between migratory and nonmigratory populations. Additionally, our research confirms previous studies which show that forewing size is significantly smaller in nonmigratory populations when compared to both migratory phenotypes. Finally, we found sexual dimorphism in forewing shape in all three groups, but for size in nonmigratory populations only. This might have been caused by reduced constraints on forewing size in nonmigratory populations.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136396948","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
George S. Slyusarev, Elizaveta K. Skalon, Victor V. Starunov
{"title":"Evolution of Orthonectida body plan","authors":"George S. Slyusarev, Elizaveta K. Skalon, Victor V. Starunov","doi":"10.1111/ede.12462","DOIUrl":"10.1111/ede.12462","url":null,"abstract":"<p>Orthonectida is an enigmatic group of animals with still uncertain phylogenetic position. Orthonectids parasitize various marine invertebrates. Their life cycle comprises a parasitic plasmodium and free-living males and females. Sexual individuals develop inside the plasmodium; after egress from the host they copulate in the external environment, and the larva, which has developed inside the female infects a new host. In a series of studied orthonectid species simplification of free-living sexual individuals can be clearly traced. The number of longitudinal and transverse muscle fibers is gradually reduced. In the nervous system, simplification is even more pronounced. The number of neurons constituting the ganglion is dramatically reduced from 200 in <i>Rhopalura ophiocomae</i> to 4–6 in <i>Intoshia variabili</i>. The peripheral nervous system undergoes gradual simplification as well. The morphological simplification is accompanied with genome reduction. However, not only genes are lost from the genome, it also undergoes compactization ensured by extreme reduction of intergenic distances, short intron sizes, and elimination of repetitive elements. The main trend in orthonectid evolution is simplification and miniaturization of free-living sexual individuals coupled with reduction and compactization of the genome.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 4","pages":""},"PeriodicalIF":2.6,"publicationDate":"2023-10-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"54228394","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Epigenetics and the evolution of form: Experimental manipulation of a chromatin modification causes species-specific changes to the craniofacial skeleton","authors":"Leah DeLorenzo, Kara E. Powder","doi":"10.1111/ede.12461","DOIUrl":"10.1111/ede.12461","url":null,"abstract":"<p>A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype–phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape in <i>Maylandia</i>, but not in <i>Tropheops</i>. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time- and species-dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species-specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12461","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41233549","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Regionalization of the vertebral column and its correlation with heart position in snakes: Implications for evolutionary pathways and morphological diversification","authors":"Paul M. Hampton, Jesse M. Meik","doi":"10.1111/ede.12460","DOIUrl":"10.1111/ede.12460","url":null,"abstract":"<p>Spinal regionalization has important implications for the evolution of vertebrate body plans. We determined the variation in the number and morphology of vertebrae across the vertebral column (i.e., vertebral formula) for 63 snake species representing 13 families using intracolumnar variation in vertebral shape. Vertebral counts were used to determine the position of the heart, pylorus, and left kidney for each species. Across all species we observed a conspicuous midthoracic transition in vertebral shape, indicating four developmental domains of the precloacal vertebral column (cervical, anterior thoracic, posterior thoracic, and lumbar). Using phylogenetic analyses, the boundary between the anterior and posterior thoracic vertebrae was correlated with heart position. No associations were found between shifts in morphology of the vertebral column and either the pylorus or left kidney. We observed that among taxa, the number of preapex and postapex vertebrae could change independently from one another and from changes in the total number of precloacal vertebrae. Ancestral state reconstruction of the preapex and postapex vertebrae illustrated several evolutionary pathways by which diversity in the vertebral column and heart position have been attained. In addition, no conspicuous pattern was observed among the heart, pylorus, or kidney indicating that their relative positions to each other evolve independently. We conclude that snakes exhibit four morphologically distinct regions of the vertebral column. We discuss the implications of the forebody and hindbody vertebral formula on the morphological diversification of snakes.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 1","pages":""},"PeriodicalIF":2.9,"publicationDate":"2023-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41119005","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}