Zachery M Farrand, Kurt E Galbreath, Katherine C Teeter
Montane landscapes present an array of abiotic challenges that drive adaptive evolution amongst organisms. These adaptations can promote habitat specialisation, which may heighten the risk of extirpation from environmental change. For example, higher metabolic rates in an endothermic species may contribute to heightened cold tolerance, whilst simultaneously limiting heat tolerance. Here, using the climate-sensitive American pika (Ochotona princeps), we test for evidence of intraspecific adaptive variation amongst environmental gradients across the Intermountain West of North America. We leveraged results from previous studies on pika adaptation to generate a custom nuclear target enrichment design to sequence several hundred candidate genes related to cold, hypoxia and dietary detoxification. We also applied a 'genome skimming' approach to sequence mitochondrial DNA. Using genotype-environment association tests, we identified rare genomic variants associated with elevation and temperature variation amongst populations. Amongst mitochondrial genes, we identified intraspecific variation in selective signals and significant changes to the amino acid property equilibrium constant, which may relate to electron transport chain efficiency. These results illustrate a complex dynamic of adaptive variation amongst O. princeps where lineages and populations have adapted to unique regional conditions. Some of the clearest signals of selection were in a genetic lineage that includes pikas of the Great Basin region, which is also where recent localised extirpations have taken place and highlights the risk of losing adaptive alleles during environmental change.
{"title":"Evidence of Intraspecific Adaptive Variation in the American Pika (Ochotona princeps) on a Continental Scale Using a Target Enrichment and Mitochondrial Genome Skimming Approach.","authors":"Zachery M Farrand, Kurt E Galbreath, Katherine C Teeter","doi":"10.1111/mec.17557","DOIUrl":"https://doi.org/10.1111/mec.17557","url":null,"abstract":"<p><p>Montane landscapes present an array of abiotic challenges that drive adaptive evolution amongst organisms. These adaptations can promote habitat specialisation, which may heighten the risk of extirpation from environmental change. For example, higher metabolic rates in an endothermic species may contribute to heightened cold tolerance, whilst simultaneously limiting heat tolerance. Here, using the climate-sensitive American pika (Ochotona princeps), we test for evidence of intraspecific adaptive variation amongst environmental gradients across the Intermountain West of North America. We leveraged results from previous studies on pika adaptation to generate a custom nuclear target enrichment design to sequence several hundred candidate genes related to cold, hypoxia and dietary detoxification. We also applied a 'genome skimming' approach to sequence mitochondrial DNA. Using genotype-environment association tests, we identified rare genomic variants associated with elevation and temperature variation amongst populations. Amongst mitochondrial genes, we identified intraspecific variation in selective signals and significant changes to the amino acid property equilibrium constant, which may relate to electron transport chain efficiency. These results illustrate a complex dynamic of adaptive variation amongst O. princeps where lineages and populations have adapted to unique regional conditions. Some of the clearest signals of selection were in a genetic lineage that includes pikas of the Great Basin region, which is also where recent localised extirpations have taken place and highlights the risk of losing adaptive alleles during environmental change.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17557"},"PeriodicalIF":4.5,"publicationDate":"2024-10-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454233","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Fernando Hernández, Román B. Vercellino, Marco Todesco, Natalia Bercovich, Daniel Alvarez, Johanne Brunet, Alejandro Presotto, Loren H. Rieseberg
A better understanding of the genetic and ecological factors underlying successful invasions is critical to mitigate the negative impacts of invasive species. Here, we study the invasion history of Helianthus annuus populations from Argentina, with particular emphasis on the role of post-introduction admixture with cultivated sunflower (also H. annuus) and climate adaptation driven by large haploblocks. We conducted genotyping-by-sequencing of samples of wild populations as well as Argentinian cultivars and compared them with wild (including related annual Helianthus species) and cultivated samples from the native range. We also characterised samples for 11 known haploblocks associated with environmental variation in native populations to test whether haploblocks contributed to invasion success. Population genomics analyses supported two independent geographic sources for Argentinian populations, the central United States and Texas, but no significant contribution of related annual Helianthus species. We found pervasive admixture with cultivated sunflower, likely as result of post-introduction hybridization. Genomic scans between invasive populations and their native sources identified multiple genomic regions of divergence, possibly indicative of selection, in the invaded range. These regions significantly overlapped between the two native-invasive comparisons and showed disproportionally high crop ancestry, suggesting that crop alleles contributed to invasion success. We did not find evidence of climate adaptation mediated by haploblocks, yet outliers of genome scans were enriched in haploblock regions and, for at least two haploblocks, the cultivar haplotype was favoured in Argentina. Our results show that admixture with cultivated sunflower played a major role in the establishment and spread of H. annuus populations in Argentina.
{"title":"Admixture With Cultivated Sunflower Likely Facilitated Establishment and Spread of Wild Sunflower (Helianthus annuus) in Argentina","authors":"Fernando Hernández, Román B. Vercellino, Marco Todesco, Natalia Bercovich, Daniel Alvarez, Johanne Brunet, Alejandro Presotto, Loren H. Rieseberg","doi":"10.1111/mec.17560","DOIUrl":"10.1111/mec.17560","url":null,"abstract":"<p>A better understanding of the genetic and ecological factors underlying successful invasions is critical to mitigate the negative impacts of invasive species. Here, we study the invasion history of <i>Helianthus annuus</i> populations from Argentina, with particular emphasis on the role of post-introduction admixture with cultivated sunflower (also <i>H. annuus</i>) and climate adaptation driven by large haploblocks. We conducted genotyping-by-sequencing of samples of wild populations as well as Argentinian cultivars and compared them with wild (including related annual <i>Helianthus</i> species) and cultivated samples from the native range. We also characterised samples for 11 known haploblocks associated with environmental variation in native populations to test whether haploblocks contributed to invasion success. Population genomics analyses supported two independent geographic sources for Argentinian populations, the central United States and Texas, but no significant contribution of related annual <i>Helianthus</i> species. We found pervasive admixture with cultivated sunflower, likely as result of post-introduction hybridization. Genomic scans between invasive populations and their native sources identified multiple genomic regions of divergence, possibly indicative of selection, in the invaded range. These regions significantly overlapped between the two native-invasive comparisons and showed disproportionally high crop ancestry, suggesting that crop alleles contributed to invasion success. We did not find evidence of climate adaptation mediated by haploblocks, yet outliers of genome scans were enriched in haploblock regions and, for at least two haploblocks, the cultivar haplotype was favoured in Argentina. Our results show that admixture with cultivated sunflower played a major role in the establishment and spread of <i>H. annuus</i> populations in Argentina.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 22","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17560","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454329","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Josephine R Paris, Flávia A Nitta Fernandes, Federica Pirri, Samuele Greco, Marco Gerdol, Alberto Pallavicini, Marine Benoiste, Clément Cornec, Lorenzo Zane, Brian Haas, Céline Le Bohec, Emiliano Trucchi
Gene expression can accelerate ecological divergence by rapidly tweaking the response of an organism to novel environments, with more divergent environments exerting stronger selection and supposedly, requiring faster adaptive responses. Organisms adapted to extreme environments provide ideal systems to test this hypothesis, particularly when compared to related species with milder ecological niches. The Emperor penguin (Aptenodytes forsteri) is the only endothermic vertebrate breeding in the harsh Antarctic winter, in stark contrast with the less cold-adapted sister species, the King penguin (A. patagonicus). Assembling the first de novo transcriptomes and analysing multi-tissue (brain, kidney, liver, muscle, skin) RNA-Seq data from natural populations of both species, we quantified the shifts in tissue-enhanced genes, co-expression gene networks, and differentially expressed genes characterising Emperor penguin adaptation to the extreme Antarctic. Our analyses revealed the crucial role played by muscle and liver in temperature homeostasis, fasting, and whole-body energy metabolism (glucose/insulin regulation, lipid metabolism, fatty acid beta-oxidation, and blood coagulation). Repatterning at the regulatory level appears as more important in the brain of the Emperor penguin, showing the lowest signature of differential gene expression, but the largest co-expression gene network shift. Nevertheless, over-expressed genes related to mTOR signalling in the brain and the liver support their central role in cold and fasting responses. Besides contributing to understanding the genetics underlying complex traits, like body energy reservoir management, our results provide a first insight into the role of gene expression in adaptation to one of the most extreme environmental conditions endured by an endotherm.
{"title":"Gene Expression Shifts in Emperor Penguin Adaptation to the Extreme Antarctic Environment.","authors":"Josephine R Paris, Flávia A Nitta Fernandes, Federica Pirri, Samuele Greco, Marco Gerdol, Alberto Pallavicini, Marine Benoiste, Clément Cornec, Lorenzo Zane, Brian Haas, Céline Le Bohec, Emiliano Trucchi","doi":"10.1111/mec.17552","DOIUrl":"https://doi.org/10.1111/mec.17552","url":null,"abstract":"<p><p>Gene expression can accelerate ecological divergence by rapidly tweaking the response of an organism to novel environments, with more divergent environments exerting stronger selection and supposedly, requiring faster adaptive responses. Organisms adapted to extreme environments provide ideal systems to test this hypothesis, particularly when compared to related species with milder ecological niches. The Emperor penguin (Aptenodytes forsteri) is the only endothermic vertebrate breeding in the harsh Antarctic winter, in stark contrast with the less cold-adapted sister species, the King penguin (A. patagonicus). Assembling the first de novo transcriptomes and analysing multi-tissue (brain, kidney, liver, muscle, skin) RNA-Seq data from natural populations of both species, we quantified the shifts in tissue-enhanced genes, co-expression gene networks, and differentially expressed genes characterising Emperor penguin adaptation to the extreme Antarctic. Our analyses revealed the crucial role played by muscle and liver in temperature homeostasis, fasting, and whole-body energy metabolism (glucose/insulin regulation, lipid metabolism, fatty acid beta-oxidation, and blood coagulation). Repatterning at the regulatory level appears as more important in the brain of the Emperor penguin, showing the lowest signature of differential gene expression, but the largest co-expression gene network shift. Nevertheless, over-expressed genes related to mTOR signalling in the brain and the liver support their central role in cold and fasting responses. Besides contributing to understanding the genetics underlying complex traits, like body energy reservoir management, our results provide a first insight into the role of gene expression in adaptation to one of the most extreme environmental conditions endured by an endotherm.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17552"},"PeriodicalIF":4.5,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454234","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Audrey M Martin, Jeff A Johnson, Robert B Berry, Matthew Carling, Carlos Martínez Del Rio
Genomic resources are valuable to examine historical demographic patterns and their effects to better inform management and conservation of threatened species. We evaluated population trends and genome-wide variation in the near-threatened Orange-breasted Falcon (Falco deiroleucus) and its more common sister species, the Bat Falcon (F. rufigularis), to explore how the two species differ in genomic diversity as influenced by their contrasting long-term demographic histories. We generated and aligned whole genome resequencing data for 12 Orange-breasted Falcons and 9 Bat Falcons to an annotated Gyrfalcon (F. rusticolus) reference genome that retained approximately 22.4 million biallelic autosomal SNPs (chromosomes 1-22). Our analyses indicated much lower genomic diversity in Orange-breasted Falcons compared to Bat Falcons. All sampled Orange-breasted Falcons were significantly more inbred than the sampled Bat Falcons, with values similar to those observed in island-mainland species comparisons. The distribution of runs of homozygosity showed variation suggesting long-term low population size and the possibility of bottlenecks in Orange-breasted Falcons contrasting with consistently larger populations in Bat Falcons. Analysis of genetic load suggests that Orange-breasted Falcons are less likely to experience inbreeding depression than Bat Falcons due to reduced inbreeding load but are at elevated risk from fixation of deleterious gene variants and perhaps a reduced adaptive potential. These genomic analyses highlight differences in the historical demography of two closely related species that have influenced their current genomic diversity and should result in differing strategies for their continued conservation.
{"title":"Contrasting Genomic Diversity and Inbreeding Levels Among Two Closely Related Falcon Species With Overlapping Geographic Distributions.","authors":"Audrey M Martin, Jeff A Johnson, Robert B Berry, Matthew Carling, Carlos Martínez Del Rio","doi":"10.1111/mec.17549","DOIUrl":"https://doi.org/10.1111/mec.17549","url":null,"abstract":"<p><p>Genomic resources are valuable to examine historical demographic patterns and their effects to better inform management and conservation of threatened species. We evaluated population trends and genome-wide variation in the near-threatened Orange-breasted Falcon (Falco deiroleucus) and its more common sister species, the Bat Falcon (F. rufigularis), to explore how the two species differ in genomic diversity as influenced by their contrasting long-term demographic histories. We generated and aligned whole genome resequencing data for 12 Orange-breasted Falcons and 9 Bat Falcons to an annotated Gyrfalcon (F. rusticolus) reference genome that retained approximately 22.4 million biallelic autosomal SNPs (chromosomes 1-22). Our analyses indicated much lower genomic diversity in Orange-breasted Falcons compared to Bat Falcons. All sampled Orange-breasted Falcons were significantly more inbred than the sampled Bat Falcons, with values similar to those observed in island-mainland species comparisons. The distribution of runs of homozygosity showed variation suggesting long-term low population size and the possibility of bottlenecks in Orange-breasted Falcons contrasting with consistently larger populations in Bat Falcons. Analysis of genetic load suggests that Orange-breasted Falcons are less likely to experience inbreeding depression than Bat Falcons due to reduced inbreeding load but are at elevated risk from fixation of deleterious gene variants and perhaps a reduced adaptive potential. These genomic analyses highlight differences in the historical demography of two closely related species that have influenced their current genomic diversity and should result in differing strategies for their continued conservation.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17549"},"PeriodicalIF":4.5,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454330","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Global inequality rooted in legacies of colonialism and uneven development can lead to systematic biases in scientific knowledge. In ecology and evolutionary biology, findings, funding and research effort are disproportionately concentrated at high latitudes, while biological diversity is concentrated at low latitudes. This discrepancy may have a particular influence in fields like phylogeography, molecular ecology and conservation genetics, where the rise of genomics has increased the cost and technical expertise required to apply state-of-the-art methods. Here, we ask whether a fundamental biogeographic pattern-the latitudinal gradient of species richness in tetrapods-is reflected in the available reference genomes, an important data resource for various applications of molecular tools for biodiversity research and conservation. We also ask whether sequencing approaches differ between the Global South and Global North, reviewing the last 5 years of conservation genetics research in four leading journals. We find that extant reference genomes are scarce relative to species richness at low latitudes and that reduced representation and whole-genome sequencing are disproportionately applied to taxa in the Global North. We conclude with recommendations to close this gap and improve international collaborations in biodiversity genomics.
{"title":"A Latitudinal Gradient of Reference Genomes.","authors":"Ethan B Linck, Carlos Daniel Cadena","doi":"10.1111/mec.17551","DOIUrl":"https://doi.org/10.1111/mec.17551","url":null,"abstract":"<p><p>Global inequality rooted in legacies of colonialism and uneven development can lead to systematic biases in scientific knowledge. In ecology and evolutionary biology, findings, funding and research effort are disproportionately concentrated at high latitudes, while biological diversity is concentrated at low latitudes. This discrepancy may have a particular influence in fields like phylogeography, molecular ecology and conservation genetics, where the rise of genomics has increased the cost and technical expertise required to apply state-of-the-art methods. Here, we ask whether a fundamental biogeographic pattern-the latitudinal gradient of species richness in tetrapods-is reflected in the available reference genomes, an important data resource for various applications of molecular tools for biodiversity research and conservation. We also ask whether sequencing approaches differ between the Global South and Global North, reviewing the last 5 years of conservation genetics research in four leading journals. We find that extant reference genomes are scarce relative to species richness at low latitudes and that reduced representation and whole-genome sequencing are disproportionately applied to taxa in the Global North. We conclude with recommendations to close this gap and improve international collaborations in biodiversity genomics.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17551"},"PeriodicalIF":4.5,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454328","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Paula Escuer, Sara Guirao-Rico, Miquel A. Arnedo, Alejandro Sánchez-Gracia, Julio Rozas
The spider genus Dysdera has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, with ~60 endemic species having originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterised by phenotypic modifications encompassing morphological, metabolic and behavioural changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, D. silvatica, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low coverage-based resequencing study of a natural population of D. silvatica from La Gomera island. Taking advantage of the new high-quality genome, we characterised genome-wide levels of nucleotide polymorphism, divergence and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. We also identified several candidate genomic regions that are potentially under positive selection, highlighting relevant biological processes, such as vision and nitrogen extraction as potential adaptation targets. These processes may ultimately drive species diversification in this genus. This pioneering study of spiders that are endemic to an oceanic archipelago lays the groundwork for broader population genomics analyses aimed at understanding the genetic mechanisms driving adaptive radiation in island ecosystems.
在加那利群岛的海洋群岛中,蜘蛛属(Dysdera)经历了显著的多样化,自群岛起源以来的 2,000 万年中,共出现了约 60 种特有物种。这种进化辐射伴随着饮食结构的巨大变化,通常表现为包括形态、新陈代谢和行为变化在内的表型改变。因此,这些特有的蜘蛛是了解进化驱动因素和确定适应性辐射基因组决定因素的绝佳模型。最近,我们首次完成了地方性物种之一 D. silvatica 的染色体组水平的基因组组装,为进化基因组学研究提供了高质量的参考序列。在这里,我们对拉戈梅拉岛的一个 D. silvatica 自然种群进行了基于低覆盖率的重测序研究。利用新的高质量基因组,我们描述了全基因组核苷酸多态性、分化和连锁不平衡水平,并推断了该种群的人口历史。我们还对最近的正选择进行了全面的全基因组扫描。我们的研究结果表明,在这一受地理限制的地方性物种中,核苷酸多样性和重组水平极高,表明历史上的有效种群规模很大。我们还发现了几个可能受到正选择的候选基因组区域,突出了相关的生物过程,如视觉和氮提取等潜在的适应目标。这些过程可能最终推动该属的物种多样化。这项对海洋群岛特有蜘蛛的开创性研究为更广泛的种群基因组学分析奠定了基础,旨在了解驱动岛屿生态系统适应性辐射的遗传机制。
{"title":"Population Genomics of Adaptive Radiations: Exceptionally High Levels of Genetic Diversity and Recombination in an Endemic Spider From the Canary Islands","authors":"Paula Escuer, Sara Guirao-Rico, Miquel A. Arnedo, Alejandro Sánchez-Gracia, Julio Rozas","doi":"10.1111/mec.17547","DOIUrl":"10.1111/mec.17547","url":null,"abstract":"<p>The spider genus <i>Dysdera</i> has undergone a remarkable diversification in the oceanic archipelago of the Canary Islands, with ~60 endemic species having originated during the 20 million years since the origin of the archipelago. This evolutionary radiation has been accompanied by substantial dietary shifts, often characterised by phenotypic modifications encompassing morphological, metabolic and behavioural changes. Hence, these endemic spiders represent an excellent model for understanding the evolutionary drivers and to pinpoint the genomic determinants underlying adaptive radiations. Recently, we achieved the first chromosome-level genome assembly of one of the endemic species, <i>D. silvatica</i>, providing a high-quality reference sequence for evolutionary genomics studies. Here, we conducted a low coverage-based resequencing study of a natural population of <i>D. silvatica</i> from La Gomera island. Taking advantage of the new high-quality genome, we characterised genome-wide levels of nucleotide polymorphism, divergence and linkage disequilibrium, and inferred the demographic history of this population. We also performed comprehensive genome-wide scans for recent positive selection. Our findings uncovered exceptionally high levels of nucleotide diversity and recombination in this geographically restricted endemic species, indicative of large historical effective population sizes. We also identified several candidate genomic regions that are potentially under positive selection, highlighting relevant biological processes, such as vision and nitrogen extraction as potential adaptation targets. These processes may ultimately drive species diversification in this genus. This pioneering study of spiders that are endemic to an oceanic archipelago lays the groundwork for broader population genomics analyses aimed at understanding the genetic mechanisms driving adaptive radiation in island ecosystems.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":"33 22","pages":""},"PeriodicalIF":4.5,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17547","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454237","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
A recent sequencing study has shown that two common Caribbean corals, Montastraea cavernosa and Siderastrea siderea, each consist of four genetically distinct lineages in the Florida Keys. These lineages are specialised to a certain depth and, to a lesser extent, to nearshore or offshore habitats. We hypothesised that the lineages' environmental specialisation is at least in part due to regulatory evolution, which would manifest as the emergence of groups of coregulated genes ('modules') demonstrating lineage-specific responses to different reef environments. Our hypothesis also predicted that genes belonging to such modules would show greater genetic divergence between lineages than other genes. Contrary to these expectations, responses of cryptic lineages to natural environmental variation were essentially the same at the genome-wide gene coexpression network level, with much fewer differences in gene expression between lineages compared to between habitats. Moreover, none of the identified coregulated gene expression modules exhibit elevated genetic divergence between lineages. Possible explanations of these unexpected results range from the leading role of algal symbionts and/or microbiome in adaptation to strong action of spatially varying selection equalising gene expression patterns despite different genetic background. We discuss how future studies could assist in discriminating between these possibilities.
{"title":"Decrypting Corals: Does Regulatory Evolution Underlie Environmental Specialisation of Coral Cryptic Lineages?","authors":"Dominique N Gallery, John P Rippe, Mikhail V Matz","doi":"10.1111/mec.17546","DOIUrl":"https://doi.org/10.1111/mec.17546","url":null,"abstract":"<p><p>A recent sequencing study has shown that two common Caribbean corals, Montastraea cavernosa and Siderastrea siderea, each consist of four genetically distinct lineages in the Florida Keys. These lineages are specialised to a certain depth and, to a lesser extent, to nearshore or offshore habitats. We hypothesised that the lineages' environmental specialisation is at least in part due to regulatory evolution, which would manifest as the emergence of groups of coregulated genes ('modules') demonstrating lineage-specific responses to different reef environments. Our hypothesis also predicted that genes belonging to such modules would show greater genetic divergence between lineages than other genes. Contrary to these expectations, responses of cryptic lineages to natural environmental variation were essentially the same at the genome-wide gene coexpression network level, with much fewer differences in gene expression between lineages compared to between habitats. Moreover, none of the identified coregulated gene expression modules exhibit elevated genetic divergence between lineages. Possible explanations of these unexpected results range from the leading role of algal symbionts and/or microbiome in adaptation to strong action of spatially varying selection equalising gene expression patterns despite different genetic background. We discuss how future studies could assist in discriminating between these possibilities.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17546"},"PeriodicalIF":4.5,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454331","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nicole M Tosto, Emily Rose, Heather D Mason, Judith E Mank, Sarah P Flanagan
Species lacking distinct secondary sex characteristics, such as differences in size or morphology, are often thought to experience lower levels of sex-specific selection in comparison to highly sexually dimorphic organisms. However, monomorphism in classic visible traits could be a result of genetic or physiological constraints that prevent the sexes from reaching divergent fitness optima. Additionally, biochemical and molecular work have revealed a variety of less easily observed phenotypes that nonetheless exhibit profound dimorphism. Sex-specific selection could act on these more subtle, less visible, traits. We investigate sex-specific selection in the polygynandrous dusky pipefish (Syngnathus floridae), which lacks distinct secondary sexual characteristics such as size, colour and morphological dimorphism. Using experimental breeding populations, we revealed that although males and females have similar opportunities for sexual selection, only males experience significant sexual selection pressures on body size. We also investigated patterns of sex-biased and sex-specific gene expression in gonads, livers and gills, and tested whether genes with highly divergent expression patterns between the sexes are more likely to be tissue-specific, and therefore relieved of genetic constraints. Sex bias in gene expression was widespread, although the reproductive organs had the most sex-biased and sex-specific genes. Sex-specific selection on gene expression in gills was primarily related to immune response, whereas the liver and gonads had a wide variety of cellular processes, as well as reproductive proteins, showing sex-biased expression. These sex-biased genes showed higher organ-specificity in their expression patterns, suggesting that pleiotropic constraints might have historically impacted the evolution of sex-specific expression patterns. Altogether, we find evidence for ongoing and historical sex-specific selection in the dusky pipefish.
{"title":"Sexual Selection on Non-Ornamental Traits Is Underpinned by Evidence of Genetic Constraints on Sex-Biased Expression in Dusky Pipefish.","authors":"Nicole M Tosto, Emily Rose, Heather D Mason, Judith E Mank, Sarah P Flanagan","doi":"10.1111/mec.17550","DOIUrl":"https://doi.org/10.1111/mec.17550","url":null,"abstract":"<p><p>Species lacking distinct secondary sex characteristics, such as differences in size or morphology, are often thought to experience lower levels of sex-specific selection in comparison to highly sexually dimorphic organisms. However, monomorphism in classic visible traits could be a result of genetic or physiological constraints that prevent the sexes from reaching divergent fitness optima. Additionally, biochemical and molecular work have revealed a variety of less easily observed phenotypes that nonetheless exhibit profound dimorphism. Sex-specific selection could act on these more subtle, less visible, traits. We investigate sex-specific selection in the polygynandrous dusky pipefish (Syngnathus floridae), which lacks distinct secondary sexual characteristics such as size, colour and morphological dimorphism. Using experimental breeding populations, we revealed that although males and females have similar opportunities for sexual selection, only males experience significant sexual selection pressures on body size. We also investigated patterns of sex-biased and sex-specific gene expression in gonads, livers and gills, and tested whether genes with highly divergent expression patterns between the sexes are more likely to be tissue-specific, and therefore relieved of genetic constraints. Sex bias in gene expression was widespread, although the reproductive organs had the most sex-biased and sex-specific genes. Sex-specific selection on gene expression in gills was primarily related to immune response, whereas the liver and gonads had a wide variety of cellular processes, as well as reproductive proteins, showing sex-biased expression. These sex-biased genes showed higher organ-specificity in their expression patterns, suggesting that pleiotropic constraints might have historically impacted the evolution of sex-specific expression patterns. Altogether, we find evidence for ongoing and historical sex-specific selection in the dusky pipefish.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":" ","pages":"e17550"},"PeriodicalIF":4.5,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142454238","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}