{"title":"Pervasive mitochondrial tRNA gene loss in the clade B of haplosclerid sponges (Porifera, Demospongiae).","authors":"Dennis V Lavrov, Thomas L Turner, Jan Vicente","doi":"10.1093/gbe/evaf020","DOIUrl":"https://doi.org/10.1093/gbe/evaf020","url":null,"abstract":"<p><p>Mitochondrial tRNA gene loss and cytosolic tRNA import are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because the mitochondrial DNA (mtDNA) of most bilaterally symmetrical animals (Bilateria) encodes a complete set of tRNAs required for mitochondrial translation. By contrast, the mtDNA of non-bilaterian animals (phyla Cnidaria, Ctenophora, Porifera, and Placozoa) often contains a reduced set of tRNA genes, necessitating tRNA import from the cytosol. Interestingly, in many non-bilaterian lineages, tRNA gene content appears to be set early in evolution and remains conserved thereafter. Here, we report that Clade B of Haplosclerid Sponges (CBHS) represents an exception to this pattern, displaying considerable variation in tRNA gene content even among relatively closely related species. We determined mt-genome sequences for eight CBHS species and analyzed them in conjunction with six previously available sequences. Additionally, we sequenced mt-genomes for two species of haplosclerid sponges outside the CBHS and used eight previously available sequences as outgroups. We found that tRNA gene content varied widely within CBHS, ranging from three in an undescribed Haliclona species (Haliclona sp. TLT785) to 25 in Xestospongia muta and X. testudinaria. Furthermore, we found that all CBHS species outside the genus Xestospongia lacked the atp9 gene, with some also lacking atp8. Analysis of nuclear sequences from Niphates digitalis revealed that both atp8 and atp9 had transferred to the nuclear genome, while the absence of mt-tRNA genes indicated their genuine loss. We argue that CBHS can serve as a valuable system for studying mt-tRNA gene loss, mitochondrial import of cytosolic tRNAs, and the impact of these processes on mitochondrial evolution.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143364429","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Reduced efficacy of selection on a young Z chromosome region of Schistosoma japonicum.","authors":"Andrea Mrnjavac, Beatriz Vicoso","doi":"10.1093/gbe/evaf021","DOIUrl":"https://doi.org/10.1093/gbe/evaf021","url":null,"abstract":"<p><p>Sex-linked and autosomal loci experience different selective pressures and evolutionary dynamics. X (or Z) chromosomes are often hemizygous in males (or females), as Y (or W) chromosomes often degenerate. Such hemizygous regions can be under greater efficacy of selection, as recessive mutations are immediately exposed to selection in the heterogametic sex leading to faster adaptation and faster divergence on the X chromosome (the so-called Faster-X or Faster-Z effect). However, in young non-recombining regions, Y/W chromosomes often have many functional genes, and many X/Z-linked loci are therefore diploid. The sheltering of recessive mutations on the X/Z by the Y/W homolog is expected to drive slower adaptation for diploid X/Z loci, i.e. a reduction in the efficacy of selection. While the Faster-X effect has been studied extensively, much less is known empirically about the evolutionary dynamics of diploid X or Z chromosomes. Here, we took advantage of published population genomic data in the female-heterogametic human parasite Schistosoma japonicum to characterize the gene content and diversity levels of the diploid and hemizygous regions of the Z chromosome. We used different metrics of selective pressures acting on genes to test for differences in the efficacy of selection in hemizygous and diploid Z regions, relative to autosomes. We found consistent patterns suggesting reduced Ne, and reduced efficacy of purifying selection, on both hemizygous and diploid Z regions. Moreover, relaxed selection was particularly pronounced for female-biased genes on the diploid Z, as predicted by recent theoretical work.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143364443","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gregg W C Thomas, Jonathan J Hughes, Tomohiro Kumon, Jacob S Berv, C Erik Nordgren, Michael Lampson, Mia Levine, Jeremy B Searle, Jeffrey M Good
{"title":"The genomic landscape, causes, and consequences of extensive phylogenomic discordance in murine rodents.","authors":"Gregg W C Thomas, Jonathan J Hughes, Tomohiro Kumon, Jacob S Berv, C Erik Nordgren, Michael Lampson, Mia Levine, Jeremy B Searle, Jeffrey M Good","doi":"10.1093/gbe/evaf017","DOIUrl":"10.1093/gbe/evaf017","url":null,"abstract":"<p><p>A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents - a large and ecologically diverse group that gave rise to the laboratory mouse and rat model systems. Combining recently published linked-read genome assemblies for seven murine species with other available rodent genomes, we first used ultra-conserved elements (UCEs) to infer a robust time-calibrated species tree. We then used whole genomes to examine finer-scale patterns of discordance across ∼12 million years of divergence. We found that proximate chromosomal regions tended to have more similar phylogenetic histories. There was no clear relationship between local tree similarity and recombination rates in house mice, but we did observe a correlation between recombination rates and average similarity to the species tree. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to appreciably less discordance. Finally, we show that assuming a single species tree can result in substantial deviation from the results with gene trees when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143188900","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jean-Baptiste Ledoux, Jessica Gomez-Garrido, Fernando Cruz, Francisco Camara Ferreira, Ana Matos, Xenia Sarropoulou, Sandra Ramirez-Calero, Didier Aurelle, Paula Lopez-Sendino, Natalie E Grayson, Bradley S Moore, Agostinho Antunes, Laura Aguilera, Marta Gut, Judit Salces-Ortiz, Rosa Fernández, Cristina Linares, Joaquim Garrabou, Tyler Alioto
{"title":"Chromosome-Level Genome Assembly and Annotation of Corallium rubrum: A Mediterranean Coral Threatened by Overharvesting and Climate Change.","authors":"Jean-Baptiste Ledoux, Jessica Gomez-Garrido, Fernando Cruz, Francisco Camara Ferreira, Ana Matos, Xenia Sarropoulou, Sandra Ramirez-Calero, Didier Aurelle, Paula Lopez-Sendino, Natalie E Grayson, Bradley S Moore, Agostinho Antunes, Laura Aguilera, Marta Gut, Judit Salces-Ortiz, Rosa Fernández, Cristina Linares, Joaquim Garrabou, Tyler Alioto","doi":"10.1093/gbe/evae253","DOIUrl":"https://doi.org/10.1093/gbe/evae253","url":null,"abstract":"<p><p>Reference genomes are key resources in biodiversity conservation. Yet, sequencing efforts are not evenly distributed across the tree of life raising concerns over our ability to enlighten conservation with genomic data. Good-quality reference genomes remain scarce in octocorals while these species are highly relevant targets for conservation. Here, we present the first annotated reference genome in the red coral, Corallium rubrum (Linnaeus, 1758), a habitat-forming octocoral from the Mediterranean and neighboring Atlantic, impacted by overharvesting and anthropogenic warming-induced mass mortality events. Combining long reads from Oxford Nanopore Technologies (ONT), Illumina paired-end reads for improving the base accuracy of the ONT-based genome assembly, and Arima Hi-C contact data to place the sequences into chromosomes, we assembled a genome of 532 Mb (20 chromosomes, 309 scaffolds) with contig and scaffold N50 of 1.6 and 18.5 Mb, respectively. Fifty percent of the sequence (L50) was contained in seven superscaffolds. The consensus quality value of the final assembly was 42, and the single and duplicated gene completeness reported by BUSCO was 86.4% and 1%, respectively (metazoa_odb10 database). We annotated 26,348 protein-coding genes and 34,548 noncoding transcripts. This annotated chromosome-level genome assembly, one of the first in octocorals and the first in Scleralcyonacea order, is currently used in a project based on whole-genome resequencing dedicated to the conservation and management of C. rubrum.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":"17 2","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143364447","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kayla Wilhoit, Shun Yamanouchi, Bo-Jyun Chen, Yo Y Yamasaki, Asano Ishikawa, Jun Inoue, Wataru Iwasaki, Jun Kitano
{"title":"Convergent Evolution and Predictability of Gene Copy Numbers Associated with Diets in Mammals.","authors":"Kayla Wilhoit, Shun Yamanouchi, Bo-Jyun Chen, Yo Y Yamasaki, Asano Ishikawa, Jun Inoue, Wataru Iwasaki, Jun Kitano","doi":"10.1093/gbe/evaf008","DOIUrl":"10.1093/gbe/evaf008","url":null,"abstract":"<p><p>Convergent evolution, the evolution of the same or similar phenotypes in phylogenetically independent lineages, is a widespread phenomenon in nature. If the genetic basis for convergent evolution is predictable to some extent, it may be possible to infer organismic phenotypes and the capability of organisms to utilize new ecological resources based on genome sequence data. While repeated amino acid changes have been studied in association with convergent evolution, relatively little is known about the potential contribution of repeated gene copy number changes. In this study, we explore whether gene copy number changes of particular gene families are linked to diet shifts in mammals and assess whether trophic ecology can be inferred from the copy numbers of a specific set of gene families. Using 86 mammalian genome sequences, we identified 24 gene families with a trend toward higher copy numbers in herbivores, carnivores, and omnivores, even after phylogenetic corrections. We were able to confirm previous findings on genes such as amylase, olfactory receptors, and xenobiotic metabolism genes, and identify novel gene families whose copy numbers correlate with dietary patterns. For example, omnivores exhibited higher copy numbers of genes encoding regulators of translation. We also established a discriminant function based on the copy numbers of 13 gene families that can help predict trophic ecology to some extent. These findings highlight a possible association between convergent evolution and repeated copy number changes in specific gene families, suggesting the potential to develop a method for predicting animal ecology from genome sequence data.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11797053/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143028634","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
John M Lemas, Eric L Patterson, Luan Cutti, Sarah Morran, Nicholas A Johnson, Jacob Montgomery, Fatemeh Abdollahi, David R Nelson, Victor Llaca, Kevin Fengler, Philip Westra, Todd A Gaines
{"title":"Assembly and Annotation of the Tetraploid Salsola tragus (Russian Thistle) Genome.","authors":"John M Lemas, Eric L Patterson, Luan Cutti, Sarah Morran, Nicholas A Johnson, Jacob Montgomery, Fatemeh Abdollahi, David R Nelson, Victor Llaca, Kevin Fengler, Philip Westra, Todd A Gaines","doi":"10.1093/gbe/evaf014","DOIUrl":"10.1093/gbe/evaf014","url":null,"abstract":"<p><p>This report presents two phased chromosome-scale genome assemblies of allotetraploid Salsola tragus (2n = 4x = 36) and fills the current genomics resource gap for this species. Flow cytometry estimated 1C genome size was 1.319 Gb. PacBio HiFi reads were assembled and scaffolded with Hi-C chromatin contact mapping and Bionano optical mapping data. For annotation, a PacBio Iso-Seq library was generated from root, stem, leaf, and floral tissues followed by annotation using a modified Maker pipeline. The assembled haploid S. tragus genomes contained 18 chromosomes each, with 9 chromosomes assigned to subgenome A and 9 chromosomes to subgenome B. Each haplome assembly represented 95% of the total flow cytometry estimated genome size. Haplome 1 and haplome 2 contained 43,354 and 42,221 annotated genes, respectively. The availability of high-quality reference genomes for this economically important weed will facilitate future omics analysis of S. tragus and a better understanding of chenopod plants.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11797066/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143038063","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carolina Diaz Arenas, Maristella Alvarez, Robert H Wilson, Eugene I Shakhnovich, C Brandon Ogbunugafor
{"title":"Protein Quality Control is a Master Modulator of Molecular Evolution in Bacteria.","authors":"Carolina Diaz Arenas, Maristella Alvarez, Robert H Wilson, Eugene I Shakhnovich, C Brandon Ogbunugafor","doi":"10.1093/gbe/evaf010","DOIUrl":"10.1093/gbe/evaf010","url":null,"abstract":"<p><p>The bacterial protein quality control (PQC) network comprises a set of genes that promote proteostasis (proteome homeostasis) through proper protein folding and function via chaperones, proteases, and protein translational machinery. It participates in vital cellular processes and influences organismal development and evolution. In this review, we examine the mechanistic bases for how the bacterial PQC network influences molecular evolution. We discuss the relevance of PQC components to contemporary issues in evolutionary biology including epistasis, evolvability, and the navigability of protein space. We examine other areas where proteostasis affects aspects of evolution and physiology, including host-parasite interactions. More generally, we demonstrate that the study of bacterial systems can aid in broader efforts to understand the relationship between genotype and phenotype across the biosphere.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11789785/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143004402","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Vasiliki Koutsouveli, Montserrat Torres-Oliva, Till Bayer, Janina Fuß, Nora Grossschmidt, Angela M Marulanda-Gomez, Nadin Jensen, Diana Gill, Ruth A Schmitz, Lucía Pita, Thorsten B H Reusch
{"title":"The Chromosome-level Genome of the Ctenophore Mnemiopsis leidyi A. Agassiz, 1865 Reveals a Unique Immune Gene Repertoire.","authors":"Vasiliki Koutsouveli, Montserrat Torres-Oliva, Till Bayer, Janina Fuß, Nora Grossschmidt, Angela M Marulanda-Gomez, Nadin Jensen, Diana Gill, Ruth A Schmitz, Lucía Pita, Thorsten B H Reusch","doi":"10.1093/gbe/evaf006","DOIUrl":"10.1093/gbe/evaf006","url":null,"abstract":"<p><p>Ctenophora are basal marine metazoans, the sister group of all other animals. Mnemiopsis leidyi is one of the most successful invasive species worldwide with intense ecological and evolutionary research interest. Here, we generated a chromosome-level genome assembly of M. leidyi with a focus on its immune gene repertoire. The genome was 247.97 Mb, with N50 16.84 Mb, and 84.7% completeness. Its karyotype was 13 chromosomes. In this genome and that of two other ctenophores, Bolinopsis microptera and Hormiphora californensis, we detected a high number of protein domains related to potential immune receptors. Among those, proteins containing Toll/interleukin-1 (TIR2) domain, NACHT domain, Scavenger Receptor Cystein-Rich (SRCR) domain, or C-type Lectin domain (CTLD) were abundant and presented unique domain architectures in M. leidyi. M. leidyi seems to lack bona fide Toll-like Receptors, but it does possess a repertoire of 15 TIR2 domain-containing genes. Besides, we detected a bona fide NOD-like receptor and 38 NACHT domain-containing genes. In order to verify the function of those domain-containing genes, we exposed M. leidyi to the pathogen Vibrio coralliilyticus. Among the differentially expressed genes, we identified potential immune receptors, including four TIR2 domain-containing genes, all of which were upregulated in response to pathogen exposure. To conclude, many common immune receptor domains, highly conserved across metazoans, are already present in Ctenophora. These domains have large expansions and unique architectures in M. leidyi, findings consistent with the basal evolutionary position of this group, but still might have conserved functions in immunity and host-microbe interaction.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11797021/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143004417","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Functional Carbohydrate-Active Enzymes Acquired by Horizontal Gene Transfer from Plants in the Whitefly Bemisia tabaci.","authors":"Dominique Colinet, Mireille Haon, Elodie Drula, Mathilde Boyer, Sacha Grisel, Carole Belliardo, Georgios D Koutsovoulos, Jean-Guy Berrin, Etienne G J Danchin","doi":"10.1093/gbe/evaf012","DOIUrl":"10.1093/gbe/evaf012","url":null,"abstract":"<p><p>Carbohydrate-active enzymes involved in the degradation of plant cell walls and/or the assimilation of plant carbohydrates for energy uptake are widely distributed in microorganisms. In contrast, they are less frequent in animals, although there are exceptions, including examples of carbohydrate-active enzymes acquired by horizontal gene transfer from bacteria or fungi in several of phytophagous arthropods and plant-parasitic nematodes. Although the whitefly Bemisia tabaci is a major agricultural pest, knowledge of horizontal gene transfer-acquired carbohydrate-active enzymes in this phloem-feeding insect of the Hemiptera order (subfamily Aleyrodinae) is still lacking. We performed a comprehensive and accurate detection of horizontal gene transfer candidates in B. tabaci and identified 136 horizontal gene transfer events, 14 of which corresponding to carbohydrate-active enzymes. The B. tabaci horizontal gene transfer-acquired carbohydrate-active enzymes were not only of bacterial or fungal origin, but some were also acquired from plants. Biochemical analysis revealed that members of the glycoside hydrolase families 17 and 152 acquired from plants are functional beta-glucanases with different substrate specificities, suggesting distinct roles. These two carbohydrate-active enzymes are the first characterized glycoside hydrolase families 17 and 152 glucanases in an animal. We identified a lower number of horizontal gene transfer events in the related Aleyrodinae Trialeurodes vaporariorum, with only three horizontal gene transfer-acquired carbohydrate-active enzymes, including a glycoside hydrolase family 152 glucanase, with phylogenetic analysis suggesting a unique horizontal gene transfer event in the ancestor of the Aleyrodinae. Another glycoside hydrolase family 152 carbohydrate-active enzyme, most likely independently acquired from plants, was also identified in two plant cell-feeding insects of the Thysanoptera order, highlighting the importance of plant-acquired carbohydrate-active enzymes in the biology of piercing-sucking insects.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11800479/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143038192","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rémi Allio, Sophie Teullet, Dave Lutgen, Amandine Magdeleine, Rachid Koual, Marie-Ka Tilak, Benoit de Thoisy, Christopher A Emerling, Tristan Lefébure, Frédéric Delsuc
{"title":"Transcriptomic Data Reveal Divergent Paths of Chitinase Evolution Underlying Dietary Convergence in Anteaters and Pangolins.","authors":"Rémi Allio, Sophie Teullet, Dave Lutgen, Amandine Magdeleine, Rachid Koual, Marie-Ka Tilak, Benoit de Thoisy, Christopher A Emerling, Tristan Lefébure, Frédéric Delsuc","doi":"10.1093/gbe/evaf002","DOIUrl":"10.1093/gbe/evaf002","url":null,"abstract":"<p><p>Ant-eating mammals represent a textbook example of convergent evolution. Among them, anteaters and pangolins exhibit the most extreme convergent phenotypes with complete tooth loss, elongated skulls, protruding tongues, and hypertrophied salivary glands producing large amounts of saliva. However, comparative genomic analyses have shown that anteaters and pangolins differ in their chitinase acidic gene (CHIA) repertoires, which potentially degrade the chitinous exoskeletons of ingested ants and termites. While the southern tamandua (Tamandua tetradactyla) harbors four functional CHIA paralogs (CHIA1-4), Asian pangolins (Manis spp.) have only one functional paralog (CHIA5). Here, we performed a comparative transcriptomic analysis of salivary glands in 33 placental species, including 16 novel transcriptomes from ant-eating species and close relatives. Our results suggest that salivary glands play an important role in adaptation to an insect-based diet, as expression of different CHIA paralogs is observed in insectivorous species. Furthermore, convergently evolved pangolins and anteaters express different chitinases in their digestive tracts. In the Malayan pangolin, CHIA5 is overexpressed in all major digestive organs, whereas in the southern tamandua, all four functional paralogs are expressed, at very high levels for CHIA1 and CHIA2 in the pancreas and for CHIA3 and CHIA4 in the salivary glands, stomach, liver, and pancreas. Overall, our results demonstrate that divergent molecular mechanisms within the chitinase acidic gene family underlie convergent adaptation to the ant-eating diet in pangolins and anteaters. This study highlights the role of historical contingency and molecular tinkering of the chitin digestive enzyme toolkit in this classic example of convergent evolution.</p>","PeriodicalId":12779,"journal":{"name":"Genome Biology and Evolution","volume":" ","pages":""},"PeriodicalIF":3.2,"publicationDate":"2025-02-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11789784/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142947771","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}