{"title":"The evolution of tenascins","authors":"Josephine C. Adams, Richard P. Tucker","doi":"10.1186/s12862-024-02306-2","DOIUrl":"https://doi.org/10.1186/s12862-024-02306-2","url":null,"abstract":"<h3 data-test=\"abstract-sub-heading\">Background</h3><p>The evolution of extracellular matrix is tightly linked to the evolution of organogenesis in metazoans. Tenascins are extracellular matrix glycoproteins of chordates that participate in integrin-signaling and morphogenetic events. Single tenascins are encoded by invertebrate chordates, and multiple tenascin paralogs are found in vertebrates (designated tenascin-C, tenascin-R, tenascin-W and tenascin-X) yet, overall, the evolution of this family has remained unclear.</p><h3 data-test=\"abstract-sub-heading\">Results</h3><p>This study examines the genomes of hemichordates, cephalochordates, tunicates, agnathans, cartilaginous fishes, lobe-finned fishes, ray-finned fishes and representative tetrapods to identify predicted tenascin proteins. We comprehensively assess their evolutionary relationships by sequence conservation, molecular phylogeny and examination of conservation of synteny of the encoding genes. The resulting new evolutionary model posits the origin of tenascin in an ancestral chordate, with tenascin-C-like and tenascin-R-like paralogs emerging after a whole genome duplication event in an ancestral vertebrate. Tenascin-X appeared following a second round of whole genome duplication in an ancestral gnathostome, most likely from duplication of the gene encoding the tenascin-R homolog. The fourth gene, encoding tenascin-W (also known as tenascin-N), apparently arose from a local duplication of <i>tenascin-R</i>.</p><h3 data-test=\"abstract-sub-heading\">Conclusions</h3><p>The diversity of tenascin paralogs observed in agnathans and gnathostomes has evolved through selective retention of novel genes that arose from a combination of whole genome and local duplication events. The evolutionary appearance of specific tenascin paralogs coincides with the appearance of vertebrate-specific cell and tissue types where the paralogs are abundantly expressed, such as the endocranium and facial skeleton (tenascin-C), an expanded central nervous system (tenascin-R), and bone (tenascin-W).</p>","PeriodicalId":520161,"journal":{"name":"BMC Ecology and Evolution","volume":"22 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142253362","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Multicellularity and increasing Reynolds number impact on the evolutionary shift in flash-induced ciliary response in Volvocales","authors":"Noriko Ueki, Ken-ichi Wakabayashi","doi":"10.1186/s12862-024-02307-1","DOIUrl":"https://doi.org/10.1186/s12862-024-02307-1","url":null,"abstract":"<h3 data-test=\"abstract-sub-heading\">Background</h3><p>Volvocales in green algae have evolved by multicellularity of <i>Chlamydomonas</i>-like unicellular ancestor. Those with various cell numbers exist, such as unicellular <i>Chlamydomonas</i>, four-celled <i>Tetrabaena</i>, and <i>Volvox</i> species with different cell numbers (~1,000, ~5,000, and ~10,000). Each cell of these organisms shares two cilia and an eyespot, which are used for swimming and photosensing. They are all freshwater microalgae but inhabit different fluid environments: unicellular species live in low Reynolds-number (<i>Re</i>) environments where viscous forces dominate, whereas multicellular species live in relatively higher <i>Re</i> where inertial forces become non-negligible. Despite significant changes in the physical environment, during the evolution of multicellularity, they maintained photobehaviors (i.e., photoshock and phototactic responses), which allows them to survive under changing light conditions.</p><h3 data-test=\"abstract-sub-heading\">Results</h3><p>In this study, we utilized high-speed imaging to observe flash-induced changes in the ciliary beating manner of 27 Volvocales strains. We classified flash-induced ciliary responses in Volvocales into four patterns: “1: temporal waveform conversion”, “2: no obvious response”, “3: pause in ciliary beating”, and “4: temporal changes in ciliary beating directions”. We found that which species exhibit which pattern depends on <i>Re</i>, which is associated with the individual size of each species rather than phylogenetic relationships.</p><h3 data-test=\"abstract-sub-heading\">Conclusions</h3><p>These results suggest that only organisms that acquired different patterns of ciliary responses survived the evolutionary transition to multicellularity with a greater number of cells while maintaining photobehaviors. This study highlights the significance of the <i>Re</i> as a selection pressure in evolution and offers insights for designing propulsion systems in biomimetic micromachines.</p>","PeriodicalId":520161,"journal":{"name":"BMC Ecology and Evolution","volume":"101 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142268926","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rebecca N. Lopez-Anido, Grant O. Batzel, Gabriela Ramirez, Yiqun Wang, Stephanie Neal, Maryna P. Lesoway, Jessica A. Goodheart, Deirdre C. Lyons
{"title":"The adult shell matrix protein repertoire of the marine snail Crepidula is dominated by conserved genes that are also expressed in larvae","authors":"Rebecca N. Lopez-Anido, Grant O. Batzel, Gabriela Ramirez, Yiqun Wang, Stephanie Neal, Maryna P. Lesoway, Jessica A. Goodheart, Deirdre C. Lyons","doi":"10.1186/s12862-024-02237-y","DOIUrl":"https://doi.org/10.1186/s12862-024-02237-y","url":null,"abstract":"<p>Mollusca is a morphologically diverse phylum, exhibiting an immense variety of calcium carbonate structures. Proteomic studies of adult shells often report high levels of rapidly-evolving, ‘novel’ shell matrix proteins (SMPs), which are hypothesized to drive shell diversification. However, relatively little is known about the phylogenetic distribution of SMPs, or about the function of individual SMPs in shell construction. To understand how SMPs contribute to shell diversification a thorough characterization of SMPs is required. Here, we build tools and a foundational understanding of SMPs in the marine gastropod species <i>Crepidula fornicata</i> and <i>Crepidula atrasolea</i> because they are genetically-enabled mollusc model organisms. First, we established a staging system of shell development in <i>C. atrasolea</i> for the first time. Next, we leveraged previous findings in <i>C. fornicata</i> combined with phylogenomic analyses of 95 metazoan species to determine the evolutionary lineage of its adult SMP repertoire. We found that 55% of <i>C. fornicata’s</i> SMPs belong to molluscan orthogroups, with 27% restricted to Gastropoda, and only 5% restricted at the species level. The low percentage of species-restricted SMPs underscores the importance of broad-taxon sampling and orthology inference approaches when determining homology of SMPs. From our transcriptome analysis, we found that the majority of <i>C. fornicata</i> SMPs that were found conserved in <i>C. atrasolea</i> were expressed in both larval and adult stages. We then selected a subset of SMPs of varying evolutionary ages for spatial-temporal analysis using in situ hybridization chain reaction (HCR) during larval shell development in <i>C. atrasolea</i>. Out of the 18 SMPs analyzed, 12 were detected in the larval shell field. These results suggest overlapping larval vs. adult SMP repertoires. Using multiplexed HCR, we observed five SMP expression patterns and three distinct cell populations within the shell field. These patterns support the idea that modular expression of SMPs could facilitate divergence of shell morphological characteristics. Collectively, these data establish an evolutionary and developmental framework in <i>Crepidula</i> that enables future comparisons of molluscan biomineralization to reveal mechanisms of shell diversification.</p>","PeriodicalId":520161,"journal":{"name":"BMC Ecology and Evolution","volume":"116 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142253361","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}