Daisuke S. Sato, Mayuko Nakamura, María Teresa Aguado, Toru Miura
{"title":"Secondary-tail formation during stolonization in the Japanese green syllid, Megasyllis nipponica","authors":"Daisuke S. Sato, Mayuko Nakamura, María Teresa Aguado, Toru Miura","doi":"10.1111/ede.12477","DOIUrl":"10.1111/ede.12477","url":null,"abstract":"<p>Benthic annelids belonging to the family Syllidae show a distinctive sexual reproduction mode called “stolonization,” in which posterior segments are transformed into a reproductive individual-like unit called a “stolon.” <i>Megasyllis nipponica</i> forms a stolon head and a secondary tail in the middle of the trunk before a stolon detaches, while, in the case of posterior amputation, posterior regeneration initiates at the wound after amputation. To understand the difference between posterior regeneration and secondary-tail formation during stolonization, detailed comparisons between the developmental processes of these two tail-formation types were performed in this study. Morphological and inner structural observations (i.e., cell proliferation and muscular/nervous development) showed that some processes of posterior regeneration, such as blastema formation and muscular/nervous regeneration at the amputation site, are missing during secondary-tail formation. In contrast, the secondary tail showed some unique features, such as the formation of ventrolateral half-tail buds that later fused in the middle and muscle/nerve branches formed before the detachment of the stolon. These novel features in the process of stolonization are suggested to be adaptive since the animals need to recover a posterior end quickly to stolonize again.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 3","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-04-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12477","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140678789","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}
Bethan Clark, Aaron Hickey, Aleksandra Marconi, Bettina Fischer, Joel Elkin, Rita Mateus, M. Emília Santos
{"title":"Developmental plasticity and variability in the formation of egg-spots, a pigmentation ornament in the cichlid Astatotilapia calliptera","authors":"Bethan Clark, Aaron Hickey, Aleksandra Marconi, Bettina Fischer, Joel Elkin, Rita Mateus, M. Emília Santos","doi":"10.1111/ede.12475","DOIUrl":"10.1111/ede.12475","url":null,"abstract":"<p>Vertebrate pigmentation patterns are highly diverse, yet we have a limited understanding of how evolutionary changes to genetic, cellular, and developmental mechanisms generate variation. To address this, we examine the formation of a sexually-selected male ornament exhibiting inter- and intraspecific variation, the egg-spot pattern, consisting of circular yellow-orange markings on the male anal fins of haplochromine cichlid fishes. We focus on <i>Astatotilapia calliptera</i>, the ancestor-type species of the Malawi cichlid adaptive radiation of over 850 species. We identify a key role for iridophores in initializing egg-spot aggregations composed of iridophore-xanthophore associations. Despite adult sexual dimorphism, aggregations initially form in both males and females, with development only diverging between the sexes at later stages. Unexpectedly, we found that the timing of egg-spot initialization is plastic. The earlier individuals are socially isolated, the earlier the aggregations form, with iridophores being the cell type that responds to changes to the social environment. Furthermore, we observe apparent competitive interactions between adjacent egg-spot aggregations, which strongly suggests that egg-spot patterning results mostly from cell-autonomous cellular interactions. Together, these results demonstrate that <i>A. calliptera</i> egg-spot development is an exciting model for investigating pigment pattern formation at the cellular level in a system with developmental plasticity, sexual dimorphism, and intraspecific variation. As <i>A. calliptera</i> represents the ancestral bauplan for egg-spots, these findings provide a baseline for informed comparisons across the incredibly diverse Malawi cichlid radiation.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 3","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-03-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12475","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140329787","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":"Telencephalic eversion in embryos and early larvae of four teleost species","authors":"Mónica Folgueira, Jonathan D. W. Clarke","doi":"10.1111/ede.12474","DOIUrl":"10.1111/ede.12474","url":null,"abstract":"<p>The telencephalon of ray-finned fishes undergoes eversion, which is very different to the evagination that occurs in most other vertebrates. Ventricle morphogenesis is key to build an everted telencephalon. Thus, here we use the apical marker <i>zona occludens 1</i> to understand ventricle morphology, extension of the tela choroidea and the eversion process during early telencephalon development of four teleost species: giant danio (<i>Devario aequipinnatus</i>), blind cavefish (<i>Astyanax mexicanus</i>), medaka (<i>Oryzias latipes</i>), and paradise fish (<i>Macroposus opercularis</i>). In addition, by using immunohistochemistry against tubulin and calcium-binding proteins, we analyze the general morphology of the telencephalon, showing changes in the location and extension of the olfactory bulb and other telencephalic regions from 2 to 5 days of development. We also analyze the impact of abnormal eye and telencephalon morphogenesis on eversion, showing that <i>cyclops</i> mutants do undergo eversion despite very dramatic abnormal eye morphology. We discuss how the formation of the telencephalic ventricle in teleost fish, with its characteristic shape, is a crucial event during eversion.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 2","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-02-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12474","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139995951","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":"Deciphering the origin of developmental stability: The role of intracellular expression variability in evolutionary conservation","authors":"Yui Uchida, Masato Tsutsumi, Shunsuke Ichii, Naoki Irie, Chikara Furusawa","doi":"10.1111/ede.12473","DOIUrl":"10.1111/ede.12473","url":null,"abstract":"<p>Progress in evolutionary developmental biology (evo-devo) has deepened our understanding of how intrinsic properties of embryogenesis, along with natural selection and population genetics, shape phenotypic diversity. A focal point of recent empirical and theoretical research is the idea that highly developmentally stable phenotypes are more conserved in evolution. Previously, we demonstrated that in Japanese medaka (<i>Oryzias latipes</i>), embryonic stages and genes with high stability, estimated through whole-embryo RNA-seq, are highly conserved in subsequent generations. However, the precise origin of the stability of gene expression levels evaluated at the whole-embryo level remained unclear. Such stability could be attributed to two distinct sources: stable intracellular expression levels or spatially stable expression patterns. Here we demonstrate that stability observed in whole-embryo RNA-seq can be attributed to stability at the cellular level (low variability in gene expression at the cellular levels). We quantified the intercellular variations in expression levels and spatial gene expression patterns for seven key genes involved in patterning dorsoventral and rostrocaudal regions during early development in medaka. We evaluated intracellular variability by counting transcripts and found its significant correlation with variation observed in whole-embryo RNA-seq data. Conversely, variation in spatial gene expression patterns, assessed through intraindividual left–right asymmetry, showed no correlation. Given the previously reported correlation between stability and conservation of expression levels throughout embryogenesis, our findings suggest a potential general trend: the stability or instability of developmental systems—and the consequent evolutionary diversity—may be primarily anchored in intrinsic fundamental elements such as the variability of intracellular states.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 2","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-02-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139982755","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":"Evolutionary origin of the nervous system from Ctenophora prospective","authors":"Maria Y. Sachkova","doi":"10.1111/ede.12472","DOIUrl":"10.1111/ede.12472","url":null,"abstract":"<p>Nervous system is one of the key adaptations underlying the evolutionary success of the majority of animal groups. Ctenophores (or comb jellies) are gelatinous marine invertebrates that were probably the first lineage to diverge from the rest of animals. Due to the key phylogenetic position and multiple unique adaptations, the noncentralized nervous system of comb jellies has been in the center of the debate around the origin of the nervous system in the animal kingdom and whether it happened only once or twice. Here, we discuss the latest findings in ctenophore neuroscience and multiple challenges on the way to build a clear evolutionary picture of the origin of the nervous system.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 4","pages":""},"PeriodicalIF":2.6,"publicationDate":"2024-02-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12472","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139930721","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":"Feeding-structure morphogenesis in “rhabditid” and diplogastrid nematodes is not controlled by a conserved genetic module","authors":"Tobias Theska, Ralf J. Sommer","doi":"10.1111/ede.12471","DOIUrl":"10.1111/ede.12471","url":null,"abstract":"<p>Disentangling the evolution of the molecular processes and genetic networks that facilitate the emergence of morphological novelties is one of the main objectives in evolutionary developmental biology. Here, we investigated the evolutionary history of a gene regulatory network controlling the development of novel tooth-like feeding structures in diplogastrid nematodes. Focusing on NHR-1 and NHR-40, the two transcription factors that regulate the morphogenesis of these feeding structures in <i>Pristionchus pacificus</i>, we sought to determine whether they have a similar function in <i>Caenorhabditis elegans</i>, an outgroup species to the Diplogastridae which has typical “rhabditid” flaps instead of teeth. Contrary to our initial expectations, we found that they do not have a similar function. While both receptors are co-expressed in the tissues that produce the feeding structures in the two nematodes, genetic inactivation of either receptor had no impact on feeding-structure morphogenesis in <i>C. elegans</i>. Transcriptomic experiments revealed that NHR-1 and NHR-40 have highly species-specific regulatory targets. These results suggest two possible evolutionary scenarios: either the genetic module responsible for feeding-structure morphogenesis in Diplogastridae already existed in the last common ancestor of <i>C. elegans</i> and <i>P. pacificus</i>, and subsequently disintegrated in the former as NHR-1 and NHR-40 acquired new targets, or it evolved in conjunction with teeth in Diplogastridae. These findings indicate that feeding-structure morphogenesis is regulated by different genetic programs in <i>P. pacificus</i> and <i>C. elegans</i>, hinting at developmental systems drift during the flap-to-tooth transformation. Further research in other “rhabditid” species is needed to fully reconstruct the developmental genetic changes which facilitated the evolution of novel feeding structures in Diplogastridae.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 2","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-02-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/ede.12471","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139734838","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":"The evolution of cnidarian stinging cells supports a Precambrian radiation of animal predators","authors":"Noémie C. Sierra, David A. Gold","doi":"10.1111/ede.12469","DOIUrl":"10.1111/ede.12469","url":null,"abstract":"<p>Cnidarians—the phylum including sea anemones, corals, jellyfish, and hydroids—are one of the oldest groups of predatory animals. Nearly all cnidarians are carnivores that use stinging cells called cnidocytes to ensnare and/or envenom their prey. However, there is considerable diversity in cnidocyte form and function. Tracing the evolutionary history of cnidocytes may therefore provide a proxy for early animal feeding strategies. In this study, we generated a time-calibrated molecular clock of cnidarians and performed ancestral state reconstruction on 12 cnidocyte types to test the hypothesis that the original cnidocyte was involved in prey capture. We conclude that the first cnidarians had only the simplest and least specialized cnidocyte type (the isorhiza) which was just as likely to be used for adhesion and/or defense as the capture of prey. A rapid diversification of specialized cnidocytes occurred through the Ediacaran (~654–574 million years ago), with major subgroups developing unique sets of cnidocytes to match their distinct feeding styles. These results are robust to changes in the molecular clock model, and are consistent with growing evidence for an Ediacaran diversification of animals. Our work also provides insight into the evolution of this complex cell type, suggesting that convergence of forms is rare, with the mastigophore being an interesting counterexample.</p>","PeriodicalId":12083,"journal":{"name":"Evolution & Development","volume":"26 2","pages":""},"PeriodicalIF":2.9,"publicationDate":"2024-01-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139485338","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}
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}