Hugo Cano-Fernández, Miguel Brun-Usan, Tazzio Tissot, Isaac Salazar-Ciudad
What morphologies are more likely to appear during evolution is a central question in zoology. Here we offer a novel approach to this question based on first developmental principles. We assumed that morphogenesis results from the genetic regulation of cell properties and behaviors (adhesion, contraction, etc.). We used EmbryoMaker, a general model of development that can simulate any gene network regulating cell properties and behaviors, the mechanical interactions and signaling between cells and the morphologies arising from those. We created spherical initial conditions with anterior and dorsal territories. We performed simulations changing the cell properties and behaviors regulated in these territories to explore which morphologies may have been possible. Thus, we obtained a set of the most basic animal morphologies that can be developmentally possible assuming very simple induction and morphogenesis. Our simulations suggest that elongation, invagination, evagination, condensation and anisotropic growth are the morphogenetic transformations more likely to appear from changes in cell properties and behaviors. We also found some parallels between our simulations and the morphologies of simple animals, some early stages of animal development and fossils attributed to early animals.
{"title":"A Morphospace Exploration Using a General Model of Development Reveals a Basic Set of Morphologies for Early Animal Development and Evolution","authors":"Hugo Cano-Fernández, Miguel Brun-Usan, Tazzio Tissot, Isaac Salazar-Ciudad","doi":"10.1002/jez.b.23279","DOIUrl":"10.1002/jez.b.23279","url":null,"abstract":"<p>What morphologies are more likely to appear during evolution is a central question in zoology. Here we offer a novel approach to this question based on first developmental principles. We assumed that morphogenesis results from the genetic regulation of cell properties and behaviors (adhesion, contraction, etc.). We used EmbryoMaker, a general model of development that can simulate any gene network regulating cell properties and behaviors, the mechanical interactions and signaling between cells and the morphologies arising from those. We created spherical initial conditions with anterior and dorsal territories. We performed simulations changing the cell properties and behaviors regulated in these territories to explore which morphologies may have been possible. Thus, we obtained a set of the most basic animal morphologies that can be developmentally possible assuming very simple induction and morphogenesis. Our simulations suggest that elongation, invagination, evagination, condensation and anisotropic growth are the morphogenetic transformations more likely to appear from changes in cell properties and behaviors. We also found some parallels between our simulations and the morphologies of simple animals, some early stages of animal development and fossils attributed to early animals.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 2","pages":"45-58"},"PeriodicalIF":1.8,"publicationDate":"2024-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23279","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142877346","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}
Marco Mundaca, Japhet Rojas, Lefney Cumilaf, Federico Jara, David Muñoz, Luis Pastenes, Marco Méndez, Lina M Tovar, Marcela Torrejón, Germán Montoya-Sanhueza, Sylvain Marcellini
Anurans are famous for having evolved a highly simplified skull through bone loss and fusion events. Nevertheless, their skeleton displays a rich morphological diversity associated with adaptations to diverse lifestyles and ecological niches. Here, we report larval skull ossification in the Andean toad Rhinella spinulosa (Bufonidae), and compare it to the phylogenetically distant genetic model organism Xenopus tropicalis (Pipidae). We find that the ossification timing of most skull bones is conserved between both species, except for the prootic and the angulosplenial that ossify at much later stages in R. spinulosa than X. tropicalis. We propose that a delayed lower jaw ossification in R. spinulosa is tightly related to the more extensive metamorphosis process observed in this species where the ventrally oriented mouth opening shifts anteriorly. We also report two conspicuous notches in the R. spinulosa frontoparietal bone mineralization front which are absent in X. tropicalis, and presumably represent evolutionary remnants of the coronal suture that separates the frontal and parietal bones in most vertebrates. As such notches have not been overtly reported in the literature, we examined the X. tropicalis sibling species Xenopus laevis, and were able to identify similar, albeit transient, indentations in the forming frontoparietal bone, suggesting that vestigial coronal sutures might exist in more frog species than anticipated. Taken together, we show that R. spinulosa represents an ideal organism to study heterochronic shifts and the mechanisms underlying cranial suture loss which drove anuran skull simplification.
{"title":"Skull Ossification in the Andean Toad Rhinella spinulosa (Bufonidae) and the Genetic Model Organism Xenopus tropicalis (Pipidae) Reveals Heterochrony Phenomena and Frontoparietal Suture Modifications.","authors":"Marco Mundaca, Japhet Rojas, Lefney Cumilaf, Federico Jara, David Muñoz, Luis Pastenes, Marco Méndez, Lina M Tovar, Marcela Torrejón, Germán Montoya-Sanhueza, Sylvain Marcellini","doi":"10.1002/jez.b.23280","DOIUrl":"https://doi.org/10.1002/jez.b.23280","url":null,"abstract":"<p><p>Anurans are famous for having evolved a highly simplified skull through bone loss and fusion events. Nevertheless, their skeleton displays a rich morphological diversity associated with adaptations to diverse lifestyles and ecological niches. Here, we report larval skull ossification in the Andean toad Rhinella spinulosa (Bufonidae), and compare it to the phylogenetically distant genetic model organism Xenopus tropicalis (Pipidae). We find that the ossification timing of most skull bones is conserved between both species, except for the prootic and the angulosplenial that ossify at much later stages in R. spinulosa than X. tropicalis. We propose that a delayed lower jaw ossification in R. spinulosa is tightly related to the more extensive metamorphosis process observed in this species where the ventrally oriented mouth opening shifts anteriorly. We also report two conspicuous notches in the R. spinulosa frontoparietal bone mineralization front which are absent in X. tropicalis, and presumably represent evolutionary remnants of the coronal suture that separates the frontal and parietal bones in most vertebrates. As such notches have not been overtly reported in the literature, we examined the X. tropicalis sibling species Xenopus laevis, and were able to identify similar, albeit transient, indentations in the forming frontoparietal bone, suggesting that vestigial coronal sutures might exist in more frog species than anticipated. Taken together, we show that R. spinulosa represents an ideal organism to study heterochronic shifts and the mechanisms underlying cranial suture loss which drove anuran skull simplification.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":" ","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-12-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142769370","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}
Vertebrates acquired various novel traits that were pivotal in their morphological evolution. Domain shuffling, rearrangements of functional domains between genes, is a key molecular mechanism in deuterostome evolution. However, comprehensive studies focusing on early vertebrates are lacking. With advancements in genomic studies, the genomes of early vertebrate groups and cyclostomes are now accessible, enabling detailed comparative analysis while considering the timing of gene acquisition during evolution. Here, we compared 22 metazoans, including four cyclostomes, to identify genes containing novel domain architectures acquired via domain-shuffling (DSO-Gs), in the common ancestor of vertebrates, gnathostomes, and cyclostomes. We found that DSO-Gs in the common ancestor of vertebrates were associated with novel vertebrate characteristics and those in the common ancestor of gnathostomes correlated with gnathostome-specific traits. Notably, several DSO-Gs acquired in common ancestors of vertebrates have been linked to myelination, a distinct characteristic of gnathostomes. Additionally, in situ hybridization revealed specific expression patterns for the three vertebrate DSO-Gs in cyclostomes, supporting their potential functions. Our findings highlight the significance of DSO-Gs in the emergence of novel traits in the common ancestors of vertebrates, gnathostomes, and cyclostomes.
{"title":"Domain-Shuffling in the Evolution of Cyclostomes and Gnathostomes","authors":"Hirofumi Kariyayama, Takeshi Kawashima, Hiroshi Wada, Haruka Ozaki","doi":"10.1002/jez.b.23282","DOIUrl":"10.1002/jez.b.23282","url":null,"abstract":"<p>Vertebrates acquired various novel traits that were pivotal in their morphological evolution. Domain shuffling, rearrangements of functional domains between genes, is a key molecular mechanism in deuterostome evolution. However, comprehensive studies focusing on early vertebrates are lacking. With advancements in genomic studies, the genomes of early vertebrate groups and cyclostomes are now accessible, enabling detailed comparative analysis while considering the timing of gene acquisition during evolution. Here, we compared 22 metazoans, including four cyclostomes, to identify genes containing novel domain architectures acquired via domain-shuffling (DSO-Gs), in the common ancestor of vertebrates, gnathostomes, and cyclostomes. We found that DSO-Gs in the common ancestor of vertebrates were associated with novel vertebrate characteristics and those in the common ancestor of gnathostomes correlated with gnathostome-specific traits. Notably, several DSO-Gs acquired in common ancestors of vertebrates have been linked to myelination, a distinct characteristic of gnathostomes. Additionally, in situ hybridization revealed specific expression patterns for the three vertebrate DSO-Gs in cyclostomes, supporting their potential functions. Our findings highlight the significance of DSO-Gs in the emergence of novel traits in the common ancestors of vertebrates, gnathostomes, and cyclostomes.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 2","pages":"59-79"},"PeriodicalIF":1.8,"publicationDate":"2024-12-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23282","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142769351","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":"In the Spotlight—Established Researcher","authors":"Néva Meyer","doi":"10.1002/jez.b.23281","DOIUrl":"10.1002/jez.b.23281","url":null,"abstract":"","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"344 1","pages":"5-6"},"PeriodicalIF":1.8,"publicationDate":"2024-11-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142750724","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}
Arjuna Rajakumar, Luigi Pontieri, Ruyan Li, Rasmus Stenbak Larsen, Angelly Vásquez-Correa, Johanne K. L. Frandsen, Ab Matteen Rafiqi, Guojie Zhang, Ehab Abouheif
Ants are one of the most ecologically and evolutionarily successful groups of animals and exhibit a remarkable degree of phenotypic diversity. This success is largely attributed to the fact that all ants are eusocial and live in colonies with a reproductive division of labor between morphologically distinct queen and worker castes. Yet, despite over a century of studies on caste determination and evolution in ants, we lack a complete ontogenetic series from egg to adult for any ant species. We, therefore, present a developmental table for the Pharaoh ant Monomorium pharaonis, a species whose colonies simultaneously produce reproductive queens and completely sterile workers. In total, M. pharaonis embryonic, larval, and pupal development lasts 45 days. During embryogenesis, the majority of developmental events are conserved between M. pharaonis and the fruit fly Drosophila melanogaster. We discovered, however, two types of same-stage embryos before gastrulation: (1) embryos with internalized germ cells; and (2) embryos with germ cells outside of the blastoderm at the posterior pole. Moreover, we also found two-types of embryos following germ band extension: (1) embryos with primordial germ cells that will develop into reproductive queens; and (2) embryos with no germ cells that will develop into completely sterile workers. Together, these data show that queen and worker castes are already determined and differentiated by early embryogenesis. During larval development, we confirmed that reproductive and worker larvae proceed through three larval instars. Using anatomical and developmental markers, we can further discern the development of gyne (unmated queen) larvae, male larvae, and worker larvae as early as the 1st instar. Overall, we hope that the ontogenetic series we present here will serve as a blueprint for the generation of future ant developmental tables.
{"title":"From Egg to Adult: A Developmental Table of the Ant Monomorium pharaonis","authors":"Arjuna Rajakumar, Luigi Pontieri, Ruyan Li, Rasmus Stenbak Larsen, Angelly Vásquez-Correa, Johanne K. L. Frandsen, Ab Matteen Rafiqi, Guojie Zhang, Ehab Abouheif","doi":"10.1002/jez.b.23278","DOIUrl":"https://doi.org/10.1002/jez.b.23278","url":null,"abstract":"<p>Ants are one of the most ecologically and evolutionarily successful groups of animals and exhibit a remarkable degree of phenotypic diversity. This success is largely attributed to the fact that all ants are eusocial and live in colonies with a reproductive division of labor between morphologically distinct queen and worker castes. Yet, despite over a century of studies on caste determination and evolution in ants, we lack a complete ontogenetic series from egg to adult for any ant species. We, therefore, present a developmental table for the Pharaoh ant <i>Monomorium pharaonis</i>, a species whose colonies simultaneously produce reproductive queens and completely sterile workers. In total, <i>M</i>. <i>pharaonis</i> embryonic, larval, and pupal development lasts 45 days. During embryogenesis, the majority of developmental events are conserved between <i>M</i>. <i>pharaonis</i> and the fruit fly <i>Drosophila melanogaster</i>. We discovered, however, two types of same-stage embryos before gastrulation: (1) embryos with internalized germ cells; and (2) embryos with germ cells outside of the blastoderm at the posterior pole. Moreover, we also found two-types of embryos following germ band extension: (1) embryos with primordial germ cells that will develop into reproductive queens; and (2) embryos with no germ cells that will develop into completely sterile workers. Together, these data show that queen and worker castes are already determined and differentiated by early embryogenesis. During larval development, we confirmed that reproductive and worker larvae proceed through three larval instars. Using anatomical and developmental markers, we can further discern the development of gyne (unmated queen) larvae, male larvae, and worker larvae as early as the 1st instar. Overall, we hope that the ontogenetic series we present here will serve as a blueprint for the generation of future ant developmental tables.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"342 8","pages":"557-585"},"PeriodicalIF":1.8,"publicationDate":"2024-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23278","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142708375","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}
Caroline Rocher, Amélie Vernale, Laura Fierro-Constaín, Nina Séjourné, Sandrine Chenesseau, Christian Marschal, Julien Issartel, Emilie Le Goff, David Stroebel, Julie Jouvion, Morgan Dutilleul, Cédric Matthews, Florent Marschal, Nicolas Brouilly, Dominique Massey-Harroche, Quentin Schenkelaars, Alexander Ereskovsky, André Le Bivic, Emmanuelle Renard, Carole Borchiellini
The comparative study of the four non-bilaterian phyla (Cnidaria, Placozoa, Ctenophora, and Porifera) provides insights into the origin of bilaterian traits. To complete our knowledge of the cell biology and development of these animals, additional non-bilaterian models are needed. Given the developmental, histological, ecological, and genomic differences between the four sponge classes (Demospongiae, Calcarea, Homoscleromorpha, and Hexactinellida), we have been developing the Oscarella lobularis (Porifera, class Homoscleromorpha) model over the past 15 years. Here, we report a new step forward by inducing, producing, and maintaining in vitro thousands of clonal buds that now make possible various downstream applications. This study provides a full description of bud morphology, physiology, cells and tissues, from their formation to their development into juveniles, using adapted cell staining protocols. In addition, we show that buds have outstanding capabilities of regeneration after being injured and of re-epithelization after complete cell dissociation. Altogether, Oscarella buds constitute a relevant all-in-one sponge model to access a large set of biological processes, including somatic morphogenesis, epithelial morphogenesis, cell fate, body axes formation, nutrition, contraction, ciliary beating, and respiration.
{"title":"The Buds of Oscarella lobularis (Porifera, Homoscleromorpha): A New Convenient Model for Sponge Cell and Evolutionary Developmental Biology","authors":"Caroline Rocher, Amélie Vernale, Laura Fierro-Constaín, Nina Séjourné, Sandrine Chenesseau, Christian Marschal, Julien Issartel, Emilie Le Goff, David Stroebel, Julie Jouvion, Morgan Dutilleul, Cédric Matthews, Florent Marschal, Nicolas Brouilly, Dominique Massey-Harroche, Quentin Schenkelaars, Alexander Ereskovsky, André Le Bivic, Emmanuelle Renard, Carole Borchiellini","doi":"10.1002/jez.b.23271","DOIUrl":"10.1002/jez.b.23271","url":null,"abstract":"<p>The comparative study of the four non-bilaterian phyla (Cnidaria, Placozoa, Ctenophora, and Porifera) provides insights into the origin of bilaterian traits. To complete our knowledge of the cell biology and development of these animals, additional non-bilaterian models are needed. Given the developmental, histological, ecological, and genomic differences between the four sponge classes (Demospongiae, Calcarea, Homoscleromorpha, and Hexactinellida), we have been developing the <i>Oscarella lobularis</i> (Porifera, class Homoscleromorpha) model over the past 15 years. Here, we report a new step forward by inducing, producing, and maintaining in vitro thousands of clonal buds that now make possible various downstream applications. This study provides a full description of bud morphology, physiology, cells and tissues, from their formation to their development into juveniles, using adapted cell staining protocols. In addition, we show that buds have outstanding capabilities of regeneration after being injured and of re-epithelization after complete cell dissociation. Altogether, <i>Oscarella</i> buds constitute a relevant all-in-one sponge model to access a large set of biological processes, including somatic morphogenesis, epithelial morphogenesis, cell fate, body axes formation, nutrition, contraction, ciliary beating, and respiration.</p>","PeriodicalId":15682,"journal":{"name":"Journal of experimental zoology. Part B, Molecular and developmental evolution","volume":"342 8","pages":"503-528"},"PeriodicalIF":1.8,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jez.b.23271","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142372014","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}