Pub Date : 2024-09-12DOI: 10.1038/s41437-024-00724-y
David N. Fisher, Jesper Bechsgaard, Trine Bilde
Living at high density and with low genetic diversity are factors that should both increase the susceptibility of organisms to disease. Therefore, group living organisms, especially those that are inbred, should be especially vulnerable to infection and therefore have particular strategies to cope with infection. Phenotypic plasticity, underpinned by epigenetic changes, could allow group living organisms to rapidly respond to infection challenges. To explore the potential role of epigenetic modifications in the immune response to a group-living species with low genetic diversity, we compared the genome-wide DNA methylation profiles of five colonies of social spiders (Stegodyphus dumicola) in their natural habitat in Namibia at the point just before they succumbed to infection to a point at least six months previously where they were presumably healthier. We found increases in genome- and chromosome-wide methylation levels in the CpG, CHG, and CHH contexts, although the genome-wide changes were not clearly different from zero. These changes were most prominent in the CHG context, especially at a narrow region of chromosome 13, hinting at an as-of-yet unsuspected role of this DNA methylation context in phenotypic plasticity. However, there were few clear patterns of differential methylation at the base level, and genes with a known immune function in spiders had mean methylation changes close to zero. Our results suggest that DNA methylation may change with infection at large genomic scales, but that this type of epigenetic change is not necessarily integral to the immune response of social spiders.
生活在高密度和低遗传多样性环境中的生物对疾病的易感性都会增加。因此,群居生物,尤其是那些近亲繁殖的生物,应该特别容易受到感染,并因此拥有应对感染的特殊策略。表型可塑性以表观遗传变化为基础,可使群居生物快速应对感染挑战。为了探索表观遗传修饰在对遗传多样性较低的群居物种的免疫反应中可能发挥的作用,我们比较了纳米比亚自然栖息地中五群社会蜘蛛(Stegodyphus dumicola)的全基因组 DNA 甲基化图谱。我们发现,在 CpG、CHG 和 CHH 背景下,基因组和整个染色体的甲基化水平都有所增加,尽管整个基因组的变化与零没有明显差异。这些变化在 CHG 上下文中最为突出,尤其是在 13 号染色体的一个狭窄区域,这暗示了这种 DNA 甲基化上下文在表型可塑性中尚未被发现的作用。然而,在碱基水平上几乎没有明显的甲基化差异模式,而且已知具有蜘蛛免疫功能的基因的平均甲基化变化接近于零。我们的研究结果表明,DNA甲基化可能会随着大基因组尺度的感染而发生变化,但这种类型的表观遗传变化并不一定与社会蜘蛛的免疫反应密不可分。
{"title":"Exploring changes in social spider DNA methylation profiles in all cytosine contexts following infection","authors":"David N. Fisher, Jesper Bechsgaard, Trine Bilde","doi":"10.1038/s41437-024-00724-y","DOIUrl":"https://doi.org/10.1038/s41437-024-00724-y","url":null,"abstract":"<p>Living at high density and with low genetic diversity are factors that should both increase the susceptibility of organisms to disease. Therefore, group living organisms, especially those that are inbred, should be especially vulnerable to infection and therefore have particular strategies to cope with infection. Phenotypic plasticity, underpinned by epigenetic changes, could allow group living organisms to rapidly respond to infection challenges. To explore the potential role of epigenetic modifications in the immune response to a group-living species with low genetic diversity, we compared the genome-wide DNA methylation profiles of five colonies of social spiders (<i>Stegodyphus dumicola</i>) in their natural habitat in Namibia at the point just before they succumbed to infection to a point at least six months previously where they were presumably healthier. We found increases in genome- and chromosome-wide methylation levels in the CpG, CHG, and CHH contexts, although the genome-wide changes were not clearly different from zero. These changes were most prominent in the CHG context, especially at a narrow region of chromosome 13, hinting at an as-of-yet unsuspected role of this DNA methylation context in phenotypic plasticity. However, there were few clear patterns of differential methylation at the base level, and genes with a known immune function in spiders had mean methylation changes close to zero. Our results suggest that DNA methylation may change with infection at large genomic scales, but that this type of epigenetic change is not necessarily integral to the immune response of social spiders.</p>","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.8,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142200831","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}
Pub Date : 2024-09-12DOI: 10.1038/s41437-024-00722-0
Paul F. Rugman-Jones, Christine E. Dodge, Richard Stouthamer
Heteroplasmy, the presence of multiple mitochondrial genotypes (mitotypes) within an individual, has long been thought to be a rare aberrance that is quickly removed by selection or drift. However, heteroplasmy is being reported in natural populations of eukaryotes with increasing frequency, in part due to improved diagnostic methods. Here, we report a seemingly stable heteroplasmic state in California populations of the polyphagous shothole borer (PSHB), Euwallacea fornicatus; an invasive ambrosia beetle that is causing significant tree dieback. We develop and validate a qPCR assay utilizing locked nucleic acid probes to detect different mitotypes, and qualitatively assess heteroplasmy in individual PSHB. We prove the utility of this assay by: (1) mitotyping field-collected PSHB, documenting the prevalence of heteroplasmy across its range in California; and, (2) measuring relative titers of each mitotype across multiple generations of heteroplasmic laboratory colonies to assess the stability of transmission through the maternal germline. We show that our findings are unlikely to be explained by the existence of NUMTs by next generation sequencing of contiguous sections of mitochondrial DNA, where each of the observed heteroplasmic sites are found within fully functional coding regions of mtDNA. Subsequently, we find heteroplasmic individuals are common in Californian field populations, and that heteroplasmy persists for at least 10 generations in experimental colonies. We also looked for evidence of the common occurrence of paternal leakage, but found none. In light of our results, we discuss competing hypotheses as to how heteroplasmy may have arisen, and continues to perpetuate, in Californian PSHB populations.
{"title":"Pervasive heteroplasmy in an invasive ambrosia beetle (Scolytinae) in southern California","authors":"Paul F. Rugman-Jones, Christine E. Dodge, Richard Stouthamer","doi":"10.1038/s41437-024-00722-0","DOIUrl":"https://doi.org/10.1038/s41437-024-00722-0","url":null,"abstract":"<p>Heteroplasmy, the presence of multiple mitochondrial genotypes (mitotypes) within an individual, has long been thought to be a rare aberrance that is quickly removed by selection or drift. However, heteroplasmy is being reported in natural populations of eukaryotes with increasing frequency, in part due to improved diagnostic methods. Here, we report a seemingly stable heteroplasmic state in California populations of the polyphagous shothole borer (PSHB), <i>Euwallacea fornicatus</i>; an invasive ambrosia beetle that is causing significant tree dieback. We develop and validate a qPCR assay utilizing locked nucleic acid probes to detect different mitotypes, and qualitatively assess heteroplasmy in individual PSHB. We prove the utility of this assay by: (1) mitotyping field-collected PSHB, documenting the prevalence of heteroplasmy across its range in California; and, (2) measuring relative titers of each mitotype across multiple generations of heteroplasmic laboratory colonies to assess the stability of transmission through the maternal germline. We show that our findings are unlikely to be explained by the existence of NUMTs by next generation sequencing of contiguous sections of mitochondrial DNA, where each of the observed heteroplasmic sites are found within fully functional coding regions of mtDNA. Subsequently, we find heteroplasmic individuals are common in Californian field populations, and that heteroplasmy persists for at least 10 generations in experimental colonies. We also looked for evidence of the common occurrence of paternal leakage, but found none. In light of our results, we discuss competing hypotheses as to how heteroplasmy may have arisen, and continues to perpetuate, in Californian PSHB populations.</p>","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.8,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142200854","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}
Pub Date : 2024-09-12DOI: 10.1038/s41437-024-00716-y
Thomas J. McGreevy Jr., Nicholas G. Crawford, Pierre Legreneur, Christopher J. Schneider
Lizards in the genus Anolis comprise hundreds of species that display a wide range of phenotypic variation closely related to their environment. One example is the Guadeloupean anole (Anolis marmoratus ssp.) that display extreme phenotypic variation, primarily in adult male color and pattern, with twelve described subspecies on the archipelago. Here we examine the relationship between phenotypic and genetic divergence among five subspecies on the two main islands and test the role of geographic isolation and the environment in reducing gene flow. We also examined two offshore island populations to assess the impact of complete geographic isolation on gene flow. We analyzed color phenotypes by measuring spectral reflectance and genomic diversity using SNPs. Genetic divergence was correlated with dorsolateral head and body color phenotypes, and slope and geographic distance were nearly equivalent at explaining this divergence. There was minimal genome-wide divergence at neutral loci among phenotypically disparate subspecies on the two main islands and their differentiation is consistent with a model of divergence with gene flow. Our spatial visualization of gene flow showed an impact of environmental features consistent with a hypothesis of ecologically driven divergence. Nonetheless, subspecies on the two main islands remain interconnected by substantial gene flow and their phenotypic variation is likely maintained at selection-gene flow equilibrium by divergent selection at loci associated with their color phenotypes. Greater isolation, such as inhabiting a remote island, may be required for reducing gene flow. Our findings highlight the role of the environment, adaptation, and geographic isolation on gene flow.
{"title":"Influence of geographic isolation and the environment on gene flow among phenotypically diverse lizards","authors":"Thomas J. McGreevy Jr., Nicholas G. Crawford, Pierre Legreneur, Christopher J. Schneider","doi":"10.1038/s41437-024-00716-y","DOIUrl":"10.1038/s41437-024-00716-y","url":null,"abstract":"Lizards in the genus Anolis comprise hundreds of species that display a wide range of phenotypic variation closely related to their environment. One example is the Guadeloupean anole (Anolis marmoratus ssp.) that display extreme phenotypic variation, primarily in adult male color and pattern, with twelve described subspecies on the archipelago. Here we examine the relationship between phenotypic and genetic divergence among five subspecies on the two main islands and test the role of geographic isolation and the environment in reducing gene flow. We also examined two offshore island populations to assess the impact of complete geographic isolation on gene flow. We analyzed color phenotypes by measuring spectral reflectance and genomic diversity using SNPs. Genetic divergence was correlated with dorsolateral head and body color phenotypes, and slope and geographic distance were nearly equivalent at explaining this divergence. There was minimal genome-wide divergence at neutral loci among phenotypically disparate subspecies on the two main islands and their differentiation is consistent with a model of divergence with gene flow. Our spatial visualization of gene flow showed an impact of environmental features consistent with a hypothesis of ecologically driven divergence. Nonetheless, subspecies on the two main islands remain interconnected by substantial gene flow and their phenotypic variation is likely maintained at selection-gene flow equilibrium by divergent selection at loci associated with their color phenotypes. Greater isolation, such as inhabiting a remote island, may be required for reducing gene flow. Our findings highlight the role of the environment, adaptation, and geographic isolation on gene flow.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00716-y.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142200855","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}
The year 2020 was a landmark year for wheat. The wheat HB4 event harboring a drought-resistant gene from sunflowers, received regulatory approval and was grown commercially in Argentina, with approval for food and feed in other countries. This, indeed, is many years after the adoption of genetic modifications in other crops. The lack of consumer acceptance and resulting trade barriers halted the commercialization of the earliest events and had a chilling effect on, especially, private Research & Development (R&D) investments. As regulations for modern breeding technologies such as genome-edited cultivars are being discussed and/or adopted across the globe, we would like to propose a framework to ensure that wheat is not left behind a second time as the potential benefits far outweigh the perceived risks. In this paper, after a review of the technical challenges wheat faces with the generation of trans- and cis-genic wheat varieties, we discuss some of the factors that could help demystify the risk/reward equation and thereby the consumer's reluctance or acceptance of these techniques for future wheat improvement. The advent of next-generation sequencing is shedding light on natural gene transfer between species and the number of perturbations other accepted techniques like mutagenesis create. The transition from classic breeding techniques and embracing transgenic, cisgenic, and genome editing approaches feels inevitable for wheat improvement if we are to develop climate-resilient wheat varieties to feed a growing world population.
{"title":"Facts, uncertainties, and opportunities in wheat molecular improvement.","authors":"Fariba Rafiei, Jochum Wiersma, Steve Scofield, Cankui Zhang, Houshang Alizadeh, Mohsen Mohammadi","doi":"10.1038/s41437-024-00721-1","DOIUrl":"https://doi.org/10.1038/s41437-024-00721-1","url":null,"abstract":"<p><p>The year 2020 was a landmark year for wheat. The wheat HB4 event harboring a drought-resistant gene from sunflowers, received regulatory approval and was grown commercially in Argentina, with approval for food and feed in other countries. This, indeed, is many years after the adoption of genetic modifications in other crops. The lack of consumer acceptance and resulting trade barriers halted the commercialization of the earliest events and had a chilling effect on, especially, private Research & Development (R&D) investments. As regulations for modern breeding technologies such as genome-edited cultivars are being discussed and/or adopted across the globe, we would like to propose a framework to ensure that wheat is not left behind a second time as the potential benefits far outweigh the perceived risks. In this paper, after a review of the technical challenges wheat faces with the generation of trans- and cis-genic wheat varieties, we discuss some of the factors that could help demystify the risk/reward equation and thereby the consumer's reluctance or acceptance of these techniques for future wheat improvement. The advent of next-generation sequencing is shedding light on natural gene transfer between species and the number of perturbations other accepted techniques like mutagenesis create. The transition from classic breeding techniques and embracing transgenic, cisgenic, and genome editing approaches feels inevitable for wheat improvement if we are to develop climate-resilient wheat varieties to feed a growing world population.</p>","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-09-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142139886","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}
Pub Date : 2024-09-02DOI: 10.1038/s41437-024-00710-4
Christopher D. Barratt, Kathleen Preißler, Pauline R. Jennert, Falk Eckhardt, Mirjam Nadjafzadeh, Sebastian Steinfartz
Anthropogenic habitat modification and climate change are fundamental drivers of biodiversity declines, reducing the evolutionary potential of species, particularly at their distributional limits. Supportive breeding or reintroductions of individuals are often made to replenish declining populations, sometimes informed by genetic analysis. However, most approaches utilised (i.e. single locus markers) do not have the resolution to account for local adaptation to environmental conditions, a crucial aspect to consider when selecting donor and recipient populations. Here, we incorporate genetic (microsatellite) and genome-wide SNP (ddRAD-seq) markers, accounting for both neutral and putative adaptive genetic diversity, to inform the conservation management of the threatened common midwife toad, Alytes obstetricans at the northern and eastern edges of its range in Europe. We find geographically structured populations (n = 4), weak genetic differentiation and fairly consistent levels of genetic diversity across localities (observed heterozygosity and allelic richness). Categorising individuals based on putatively adaptive regions of the genome showed that the majority of localities are not strongly locally adapted. However, several localities present high numbers of private alleles in tandem with local adaptation to warmer conditions and rough topography. Combining genetic diversity and local adaptations with estimates of migration rates, we develop a decision-making framework for selecting donor and recipient populations which maximises the geographic dispersal of neutral and putatively adaptive genetic diversity. Our framework is generally applicable to any species, but especially to amphibians, so armed with this information, conservationists may avoid the reintroduction of unsuitable/maladapted individuals to new sites and increase the evolutionary potential of populations within species.
{"title":"A decision-making framework to maximise the evolutionary potential of populations - Genetic and genomic insights from the common midwife toad (Alytes obstetricans) at its range limits","authors":"Christopher D. Barratt, Kathleen Preißler, Pauline R. Jennert, Falk Eckhardt, Mirjam Nadjafzadeh, Sebastian Steinfartz","doi":"10.1038/s41437-024-00710-4","DOIUrl":"10.1038/s41437-024-00710-4","url":null,"abstract":"Anthropogenic habitat modification and climate change are fundamental drivers of biodiversity declines, reducing the evolutionary potential of species, particularly at their distributional limits. Supportive breeding or reintroductions of individuals are often made to replenish declining populations, sometimes informed by genetic analysis. However, most approaches utilised (i.e. single locus markers) do not have the resolution to account for local adaptation to environmental conditions, a crucial aspect to consider when selecting donor and recipient populations. Here, we incorporate genetic (microsatellite) and genome-wide SNP (ddRAD-seq) markers, accounting for both neutral and putative adaptive genetic diversity, to inform the conservation management of the threatened common midwife toad, Alytes obstetricans at the northern and eastern edges of its range in Europe. We find geographically structured populations (n = 4), weak genetic differentiation and fairly consistent levels of genetic diversity across localities (observed heterozygosity and allelic richness). Categorising individuals based on putatively adaptive regions of the genome showed that the majority of localities are not strongly locally adapted. However, several localities present high numbers of private alleles in tandem with local adaptation to warmer conditions and rough topography. Combining genetic diversity and local adaptations with estimates of migration rates, we develop a decision-making framework for selecting donor and recipient populations which maximises the geographic dispersal of neutral and putatively adaptive genetic diversity. Our framework is generally applicable to any species, but especially to amphibians, so armed with this information, conservationists may avoid the reintroduction of unsuitable/maladapted individuals to new sites and increase the evolutionary potential of populations within species.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41437-024-00710-4.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142119676","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}
Pub Date : 2024-08-22DOI: 10.1038/s41437-024-00718-w
Gabriel Weijie Low, Alexandra Pavlova, Han Ming Gan, Meng-Ching Ko, Keren R. Sadanandan, Yin Peng Lee, J. Nevil Amos, Lana Austin, Stephanie Falk, Damian K. Dowling, Paul Sunnucks
There is considerable evidence for mitochondrial-nuclear co-adaptation as a key evolutionary driver. Hypotheses regarding the roles of sex-linkage have emphasized Z-linked nuclear genes with mitochondrial function (N-mt genes), whereas it remains contentious whether the perfect co-inheritance of W genes with mitogenomes could hinder or facilitate co-adaptation. Young (neo-) sex chromosomes that possess relatively many N-mt genes compared to older chromosomes provide unprecedented hypothesis-testing opportunities. Eastern Yellow Robin (EYR) lineages in coastal and inland habitats with different climates are diverged in mitogenomes, and in a ~ 15.4 Mb nuclear region enriched with N-mt genes, in contrast with otherwise-similar nuclear genomes. This nuclear region maps to passerine chromosome 1A, previously found to be neo-sex in the inland EYR genome. To compare sex-linked Chr1A-derived genes between lineages, we assembled and annotated the coastal EYR genome. We found that: (i) the coastal lineage shares a similar neo-sex system with the inland lineage, (ii) neo-W and neo-Z N-mt genes are not more diverged between lineages than are comparable non-N-mt genes, and showed little evidence for broad positive selection, (iii) however, W-linked N-mt genes are more diverged between lineages than are their Z-linked gametologs. The latter effect was ~7 times stronger for N-mt than non-N-mt genes, suggesting that W-linked N-mt genes might have diverged between lineages under environmental selection through co-evolution with mitogenomes. Finally, we identify a candidate gene driver for divergent selection, NDUFA12. Our data represent a rare example suggesting a possible role for W-associated mitochondrial-nuclear interactions in climate-associated adaptation and lineage differentiation.
有大量证据表明,线粒体-核共同适应是进化的关键驱动力。有关性连锁作用的假说强调了具有线粒体功能的 Z 连锁核基因(N-mt 基因),而 W 基因与有丝分裂基因组的完美共遗传是否会阻碍或促进共同适应,仍然存在争议。与较老的染色体相比,年轻(新)的性染色体拥有相对较多的 N-mt 基因,这为我们提供了前所未有的假设检验机会。在气候不同的沿海和内陆栖息地,东方黄罗宾(EYR)种系在有丝分裂基因组和一个富含N-mt基因的约15.4 Mb核区上存在差异,这与其他相似的核基因组形成了鲜明对比。该核区域映射到传粉动物的 1A 染色体,以前曾发现该染色体在内陆 EYR 基因组中具有新性别。为了比较不同种系之间的性连锁 Chr1A 衍生基因,我们对沿海 EYR 基因组进行了组装和注释。我们发现(i) 沿岸品系与内陆品系具有相似的新性别系统;(ii) 新 W 和新 Z N-mt 基因在不同品系之间的差异并不比可比的非 N-mt 基因大,而且几乎没有证据表明存在广泛的正选择;(iii) 然而,W 连锁 N-mt 基因在不同品系之间的差异比 Z 连锁配子基因大。后者对 N-mt 基因的影响是非 N-mt 基因的 7 倍,这表明 W 连锁 N-mt 基因可能是在环境选择下通过与有丝分裂基因组共同进化而在不同种系之间发生分化的。最后,我们发现了一个驱动分化选择的候选基因--NDUFA12。我们的数据代表了一个罕见的例子,表明与 W 相关的线粒体-核相互作用可能在与气候相关的适应和种系分化中发挥作用。
{"title":"Accelerated differentiation of neo-W nuclear-encoded mitochondrial genes between two climate-associated bird lineages signals potential co-evolution with mitogenomes","authors":"Gabriel Weijie Low, Alexandra Pavlova, Han Ming Gan, Meng-Ching Ko, Keren R. Sadanandan, Yin Peng Lee, J. Nevil Amos, Lana Austin, Stephanie Falk, Damian K. Dowling, Paul Sunnucks","doi":"10.1038/s41437-024-00718-w","DOIUrl":"10.1038/s41437-024-00718-w","url":null,"abstract":"There is considerable evidence for mitochondrial-nuclear co-adaptation as a key evolutionary driver. Hypotheses regarding the roles of sex-linkage have emphasized Z-linked nuclear genes with mitochondrial function (N-mt genes), whereas it remains contentious whether the perfect co-inheritance of W genes with mitogenomes could hinder or facilitate co-adaptation. Young (neo-) sex chromosomes that possess relatively many N-mt genes compared to older chromosomes provide unprecedented hypothesis-testing opportunities. Eastern Yellow Robin (EYR) lineages in coastal and inland habitats with different climates are diverged in mitogenomes, and in a ~ 15.4 Mb nuclear region enriched with N-mt genes, in contrast with otherwise-similar nuclear genomes. This nuclear region maps to passerine chromosome 1A, previously found to be neo-sex in the inland EYR genome. To compare sex-linked Chr1A-derived genes between lineages, we assembled and annotated the coastal EYR genome. We found that: (i) the coastal lineage shares a similar neo-sex system with the inland lineage, (ii) neo-W and neo-Z N-mt genes are not more diverged between lineages than are comparable non-N-mt genes, and showed little evidence for broad positive selection, (iii) however, W-linked N-mt genes are more diverged between lineages than are their Z-linked gametologs. The latter effect was ~7 times stronger for N-mt than non-N-mt genes, suggesting that W-linked N-mt genes might have diverged between lineages under environmental selection through co-evolution with mitogenomes. Finally, we identify a candidate gene driver for divergent selection, NDUFA12. Our data represent a rare example suggesting a possible role for W-associated mitochondrial-nuclear interactions in climate-associated adaptation and lineage differentiation.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-08-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11527876/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142035668","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}
Pub Date : 2024-08-21DOI: 10.1038/s41437-024-00717-x
Martijn A. Schenkel
Sex chromosomes carry the sex-determining locus, causing them to be differently transmitted to and from females and males. These differences lead them to be selected upon in different ways, and hence they are predicted to become enriched for sexually- and parentally-antagonistic genes. Sexually-antagonistic genes have opposing fitness effects in females versus in males; parentally-antagonistic genes have opposing fitness effects when inherited maternally versus paternally. Sexually-antagonistic selection can drive sex determination transitions, whereby an autosome pair becomes a sex chromosome pair in lieu of the ancestral sex chromosomes. Whether parentally-antagonistic selection can similarly drive sex determination transitions remains unknown. I present a model to investigate the potential for transitions in sex determination through parentally-antagonistic selection as compared to sexually-antagonistic selection. This model assumes an ancestral sex-chromosomal sex-determining locus linked to a parentally- or sexually-antagonistic gene, and an autosomal parentally- or sexually-antagonistic gene in whose vicinity a novel sex-determining gene arises. I find that parentally-antagonistic selection can promote the spread of novel sex-determining genes as well as maintain ancestral sex-determining genes when the invasion of the novel sex-determining gene would involve transitions from male to female heterogamety (or vice versa), similar to sexually-antagonistic selection. Transitions between male and female heterogamety are, however, more likely when the ancestral sex-determining locus is linked to a parentally-antagonistic locus. Consequently, parentally-antagonistic selection can enable some highly unusual evolutionary patterns not encountered in other evolutionary models of sex determination. These results provide novel insights into why some sex-determining mechanisms may be so evolutionary labile.
{"title":"Transitions in sex determination mechanisms through parental and sexual antagonism","authors":"Martijn A. Schenkel","doi":"10.1038/s41437-024-00717-x","DOIUrl":"10.1038/s41437-024-00717-x","url":null,"abstract":"Sex chromosomes carry the sex-determining locus, causing them to be differently transmitted to and from females and males. These differences lead them to be selected upon in different ways, and hence they are predicted to become enriched for sexually- and parentally-antagonistic genes. Sexually-antagonistic genes have opposing fitness effects in females versus in males; parentally-antagonistic genes have opposing fitness effects when inherited maternally versus paternally. Sexually-antagonistic selection can drive sex determination transitions, whereby an autosome pair becomes a sex chromosome pair in lieu of the ancestral sex chromosomes. Whether parentally-antagonistic selection can similarly drive sex determination transitions remains unknown. I present a model to investigate the potential for transitions in sex determination through parentally-antagonistic selection as compared to sexually-antagonistic selection. This model assumes an ancestral sex-chromosomal sex-determining locus linked to a parentally- or sexually-antagonistic gene, and an autosomal parentally- or sexually-antagonistic gene in whose vicinity a novel sex-determining gene arises. I find that parentally-antagonistic selection can promote the spread of novel sex-determining genes as well as maintain ancestral sex-determining genes when the invasion of the novel sex-determining gene would involve transitions from male to female heterogamety (or vice versa), similar to sexually-antagonistic selection. Transitions between male and female heterogamety are, however, more likely when the ancestral sex-determining locus is linked to a parentally-antagonistic locus. Consequently, parentally-antagonistic selection can enable some highly unusual evolutionary patterns not encountered in other evolutionary models of sex determination. These results provide novel insights into why some sex-determining mechanisms may be so evolutionary labile.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-08-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142008749","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}
Pub Date : 2024-08-20DOI: 10.1038/s41437-024-00715-z
Noah M. Simon, Yujin Kim, Joost Gribnau, Diana M. Bautista, James R. Dutton, Rachel B. Brem
A key goal of evolutionary genomics is to harness molecular data to draw inferences about selective forces that have acted on genomes. The field progresses in large part through the development of advanced molecular-evolution analysis methods. Here we explored the intersection between classical sequence-based tests for selection and an empirical expression-based approach, using stem cells from Mus musculus subspecies as a model. Using a test of directional, cis-regulatory evolution across genes in pathways, we discovered a unique program of induction of translation genes in stem cells of the Southeast Asian mouse M. m. castaneus relative to its sister taxa. We then mined population-genomic sequences to pursue underlying regulatory mechanisms for this expression divergence, finding robust evidence for alleles unique to M. m. castaneus at the upstream regions of the translation genes. We interpret our data under a model of changes in lineage-specific pressures across Mus musculus in stem cells with high translational capacity. Our findings underscore the rigor of integrating expression and sequence-based methods to generate hypotheses about evolutionary events from long ago.
进化基因组学的一个关键目标是利用分子数据来推断基因组的选择性作用力。这一领域的进步在很大程度上得益于先进的分子进化分析方法的发展。在这里,我们以麝亚种的干细胞为模型,探索了基于序列的经典选择测试与基于经验表达的方法之间的交叉点。通过测试通路中跨基因的定向顺式调控进化,我们发现东南亚小鼠M. m. castaneus的干细胞中翻译基因的诱导程序比其姊妹类群独特。我们随后挖掘了种群基因组序列,以探寻这种表达差异的潜在调控机制,并在翻译基因的上游区域发现了蓖麻小鼠特有等位基因的有力证据。我们根据具有高翻译能力的干细胞中整个麝香种系特异性压力变化的模型来解释我们的数据。我们的发现强调了整合基于表达和序列的方法的严谨性,从而对很久以前的进化事件提出假设。
{"title":"Stem cell transcriptional profiles from mouse subspecies reveal cis-regulatory evolution at translation genes","authors":"Noah M. Simon, Yujin Kim, Joost Gribnau, Diana M. Bautista, James R. Dutton, Rachel B. Brem","doi":"10.1038/s41437-024-00715-z","DOIUrl":"10.1038/s41437-024-00715-z","url":null,"abstract":"A key goal of evolutionary genomics is to harness molecular data to draw inferences about selective forces that have acted on genomes. The field progresses in large part through the development of advanced molecular-evolution analysis methods. Here we explored the intersection between classical sequence-based tests for selection and an empirical expression-based approach, using stem cells from Mus musculus subspecies as a model. Using a test of directional, cis-regulatory evolution across genes in pathways, we discovered a unique program of induction of translation genes in stem cells of the Southeast Asian mouse M. m. castaneus relative to its sister taxa. We then mined population-genomic sequences to pursue underlying regulatory mechanisms for this expression divergence, finding robust evidence for alleles unique to M. m. castaneus at the upstream regions of the translation genes. We interpret our data under a model of changes in lineage-specific pressures across Mus musculus in stem cells with high translational capacity. Our findings underscore the rigor of integrating expression and sequence-based methods to generate hypotheses about evolutionary events from long ago.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-08-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11527988/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142008748","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}
Pub Date : 2024-08-18DOI: 10.1038/s41437-024-00719-9
Andrea Viviana Ballén-Guapacha, Sandra Milena Ospina-Garcés, Roger Guevara, Rosa Ana Sánchez-Guillén
Reproductive Character Displacement (RCD) refers to the phenomenon of greater differences in reproductive characters between two species when they occur in sympatry compared to when they occur in allopatry to prevent maladaptive hybridization. We explored whether reinforcement of a mechanical barrier involved in the first contact point between male and female genital traits during copulation in the cross between Ischnura graellsii males and Ischnura elegans females has led to RCD, and whether it supports the lock-and-key hypothesis of genital evolution. We employed geometric morphometrics to analyze the shape and size of male and female genital traits, controlling for environmental and geographic factors. Consistent with an increase in mechanical isolation via reinforcement, we detected larger divergence in genital traits between the species in sympatry than in allopatry, and also stronger signal in females than in males. In the Northwest (NW) hybrid zone, we detected RCD in I. graellsii males and I. elegans females, while in the Northcentral (NC) hybrid zone we detected RCD only in I. elegans females and I. elegans males. The detection of RCD in both sexes of I. elegans was consistent with the lock-and-key hypothesis of genital evolution via female choice for conspecific males in this species. Our study highlights the importance of using geometric morphometrics to deal with the complexity of female reproductive structures while controlling for environmental and geographic factors to investigate RCD. This study contributes valuable insights into the dynamics of reproductive isolation mechanisms and genital coevolution.
{"title":"Reproductive character displacement: insights from genital morphometrics in damselfly hybrid zones","authors":"Andrea Viviana Ballén-Guapacha, Sandra Milena Ospina-Garcés, Roger Guevara, Rosa Ana Sánchez-Guillén","doi":"10.1038/s41437-024-00719-9","DOIUrl":"10.1038/s41437-024-00719-9","url":null,"abstract":"Reproductive Character Displacement (RCD) refers to the phenomenon of greater differences in reproductive characters between two species when they occur in sympatry compared to when they occur in allopatry to prevent maladaptive hybridization. We explored whether reinforcement of a mechanical barrier involved in the first contact point between male and female genital traits during copulation in the cross between Ischnura graellsii males and Ischnura elegans females has led to RCD, and whether it supports the lock-and-key hypothesis of genital evolution. We employed geometric morphometrics to analyze the shape and size of male and female genital traits, controlling for environmental and geographic factors. Consistent with an increase in mechanical isolation via reinforcement, we detected larger divergence in genital traits between the species in sympatry than in allopatry, and also stronger signal in females than in males. In the Northwest (NW) hybrid zone, we detected RCD in I. graellsii males and I. elegans females, while in the Northcentral (NC) hybrid zone we detected RCD only in I. elegans females and I. elegans males. The detection of RCD in both sexes of I. elegans was consistent with the lock-and-key hypothesis of genital evolution via female choice for conspecific males in this species. Our study highlights the importance of using geometric morphometrics to deal with the complexity of female reproductive structures while controlling for environmental and geographic factors to investigate RCD. This study contributes valuable insights into the dynamics of reproductive isolation mechanisms and genital coevolution.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-08-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141999774","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}
Arid ecosystems, characterized by severe water scarcity, play a crucial role in preserving Earth’s biodiversity and resources. The Tarim Basin in Northwestern China, a typical arid region isolated by the Tianshan Mountains and expansive deserts, provides a special study area for investigating how plant response and adaptation to such environments. Tamarix hispida, a species well adapted to saline-alkaline and drought conditions, dominates in the saline-alkali lands of the Tarim Basin. This study aims to examine the genetic diversity and environmental adaptation of T. hispida in the Tarim Basin. Genomic SNPs for a total of 160 individuals from 17 populations were generated using dd-RAD sequencing approach. Population genetic structure and genetic diversity were analyzed by methods including ADMIXTURE, PCA, and phylogenetic tree. Environmental association analysis (EAA) was performed using LFMM and RDA analyses. The results revealed two major genetic lineages with geographical substitution patterns from west to east, indicating significant gene flow and hybridization. Environmental factors such as Precipitation Seasonality (bio15) and Topsoil Sand Fraction (T_SAND) significantly shaped allele frequencies, supporting the species’ genetic adaptability. Several genes associated with environmental adaptation were identified and annotated, highlighting physiological and metabolic processes crucial for survival in arid conditions. The study highlights the role of geographical isolation and environmental factors in shaping genetic structure and adaptive evolution. The identified adaptive genes related to stress tolerance emphasize the species’ resilience and highlight the importance of specific physiological and metabolic pathways.
{"title":"Population genetic diversity and environmental adaptation of Tamarix hispida in the Tarim Basin, arid Northwestern China","authors":"Haowen Tian, Hongxiang Zhang, Xiaojun Shi, Wenhui Ma, Jian Zhang","doi":"10.1038/s41437-024-00714-0","DOIUrl":"10.1038/s41437-024-00714-0","url":null,"abstract":"Arid ecosystems, characterized by severe water scarcity, play a crucial role in preserving Earth’s biodiversity and resources. The Tarim Basin in Northwestern China, a typical arid region isolated by the Tianshan Mountains and expansive deserts, provides a special study area for investigating how plant response and adaptation to such environments. Tamarix hispida, a species well adapted to saline-alkaline and drought conditions, dominates in the saline-alkali lands of the Tarim Basin. This study aims to examine the genetic diversity and environmental adaptation of T. hispida in the Tarim Basin. Genomic SNPs for a total of 160 individuals from 17 populations were generated using dd-RAD sequencing approach. Population genetic structure and genetic diversity were analyzed by methods including ADMIXTURE, PCA, and phylogenetic tree. Environmental association analysis (EAA) was performed using LFMM and RDA analyses. The results revealed two major genetic lineages with geographical substitution patterns from west to east, indicating significant gene flow and hybridization. Environmental factors such as Precipitation Seasonality (bio15) and Topsoil Sand Fraction (T_SAND) significantly shaped allele frequencies, supporting the species’ genetic adaptability. Several genes associated with environmental adaptation were identified and annotated, highlighting physiological and metabolic processes crucial for survival in arid conditions. The study highlights the role of geographical isolation and environmental factors in shaping genetic structure and adaptive evolution. The identified adaptive genes related to stress tolerance emphasize the species’ resilience and highlight the importance of specific physiological and metabolic pathways.","PeriodicalId":12991,"journal":{"name":"Heredity","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-08-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141975597","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}