Genetic signatures of natural selection in a model invasive ascidian

Lin, Ya‐Ping; Chen, Yiyong; Yi, Chang-Ho; Fong, Jonathan J.; Kim, Won; Rius, Marc; Zhan, Aibin

doi:10.1038/srep44080

Cited by 20 publications

(35 citation statements)

References 61 publications

(110 reference statements)

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“…(); Lin et al. () that may have led to a high rate of false positives (Lotterhos & Whitlock, ). This nonoverlap in outlier results tests has already been observed and discussed by Mäkinen et al.…”

Section: Discussionmentioning

confidence: 99%

Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins

López

Benestan

Moore

et al. 2018

Evolutionary Applications

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Selective breeding and genetic improvement have left detectable signatures on the genomes of domestic species. The elucidation of such signatures is fundamental for detecting genomic regions of biological relevance to domestication and improving management practices. In aquaculture, domestication was carried out independently in different locations worldwide, which provides opportunities to study the parallel effects of domestication on the genome of individuals that have been selected for similar traits. In this study, we aimed to detect potential genomic signatures of domestication in two independent pairs of wild/domesticated Atlantic salmon populations of Canadian and Scottish origins, respectively. Putative genomic regions under divergent selection were investigated using a 200K SNP array by combining three different statistical methods based either on allele frequencies (LFMM, Bayescan) or haplotype differentiation (Rsb). We identified 337 and 270 SNPs potentially under divergent selection in wild and hatchery populations of Canadian and Scottish origins, respectively. We observed little overlap between results obtained from different statistical methods, highlighting the need to test complementary approaches for detecting a broad range of genomic footprints of selection. The vast majority of the outliers detected were population‐specific but we found four candidate genes that were shared between the populations. We propose that these candidate genes may play a role in the parallel process of domestication. Overall, our results suggest that genetic drift may have override the effect of artificial selection and/or point toward a different genetic basis underlying the expression of similar traits in different domesticated strains. Finally, it is likely that domestication may predominantly target polygenic traits (e.g., growth) such that its genomic impact might be more difficult to detect with methods assuming selective sweeps.

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Section: Discussionmentioning

confidence: 99%

Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins

López

Benestan

Moore

et al. 2018

Evolutionary Applications

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show abstract

“…To cover the substantial environmental gradients in habitats of C. robusta and C. intestinalis , sampling sites were selected based on our former studies (Zhan et al., , ) across four continents (Asia, Africa, Europe, and Oceania) for C. robusta and two continents (Europe and North America) for C. intestinalis (Table ; Figure ). To make it clear for further comparison between genetic and methylation data, populations of both C. robusta and C. intestinalis were named as our previous studies (Lin et al., ; Zhan et al., , ). Temperature and salinity, two crucial environmental factors affecting numerous physiological processes in marine invertebrates, have a high degree of variation at the chosen sampling sites in this study (see Lin et al., for C. robusta ; Table , for C. intestinalis ).…”

Section: Methodsmentioning

confidence: 99%

“…To make it clear for further comparison between genetic and methylation data, populations of both C. robusta and C. intestinalis were named as our previous studies (Lin et al., ; Zhan et al., , ). Temperature and salinity, two crucial environmental factors affecting numerous physiological processes in marine invertebrates, have a high degree of variation at the chosen sampling sites in this study (see Lin et al., for C. robusta ; Table , for C. intestinalis ). We chose a total of 10 populations, including five populations of C. robusta ( N = 115) and five populations of C. intestinalis ( N = 148; Table ; Figure ).…”

Section: Methodsmentioning

confidence: 99%

“…Therefore, the wide range expansion of both invasive species, particularly at the regional and continental scales, mainly is owing to human‐mediated pathways, which results in sudden shifts of habitats with varied environments. As such, these two ascidians provide good models to study mechanisms of rapid microevolution during biological invasions (Lin et al., ; Pu & Zhan, ; Zhan et al., ). Our previous study revealed significant genetic differentiation among C. robusta populations collected globally by using genomewide gene‐associated microsatellites, and genetic signatures and loci under selection were associated with varied local environmental conditions (Lin et al., ).…”

Section: Introductionmentioning

confidence: 99%

“…As such, these two ascidians provide good models to study mechanisms of rapid microevolution during biological invasions (Lin et al., ; Pu & Zhan, ; Zhan et al., ). Our previous study revealed significant genetic differentiation among C. robusta populations collected globally by using genomewide gene‐associated microsatellites, and genetic signatures and loci under selection were associated with varied local environmental conditions (Lin et al., ). Furthermore, when we analyzed the DNA methylation variation of salinity and temperature‐related genes using bisulfite sequencing at the population level, we found significant variation of DNA methylation among populations (Pu & Zhan, ).…”

Section: Introductionmentioning

confidence: 99%

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Methylation divergence of invasive Ciona ascidians: Significant population structure and local environmental influence

Lin

et al. 2018

Ecology and Evolution

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The geographical expansion of invasive species usually leads to temporary and/or permanent changes at multiple levels (genetics, epigenetics, gene expression, etc.) to acclimatize to abiotic and/or biotic stresses in novel environments. Epigenetic variation such as DNA methylation is often involved in response to diverse local environments, thus representing one crucial mechanism to promote invasion success. However, evidence is scant on the potential role of DNA methylation variation in rapid environmental response and invasion success during biological invasions. In particular, DNA methylation patterns and possible contributions of varied environmental factors to methylation differentiation have been largely unknown in many invaders, especially for invasive species in marine systems where extremely complex interactions exist between species and surrounding environments. Using the methylation‐sensitive amplification polymorphism (MSAP) technique, here we investigated population methylation structure at the genome level in two highly invasive model ascidians, Ciona robusta and C. intestinalis, collected from habitats with varied environmental factors such as temperature and salinity. We found high intrapopulation methylation diversity and significant population methylation differentiation in both species. Multiple analyses, such as variation partitioning analysis, showed that both genetic variation and environmental factors contributed to the observed DNA methylation variation. Further analyses found that 24 and 20 subepiloci were associated with temperature and/or salinity in C. robusta and C. intestinalis, respectively. All these results clearly showed significant methylation divergence among populations of both invasive ascidians, and varied local environmental factors, as well as genetic variation, were responsible for the observed DNA methylation patterns. The consistent findings in both species here suggest that DNA methylation, coupled with genetic variation, may facilitate local environmental adaptation during biological invasions, and DNA methylation variation molded by local environments may contribute to invasion success.

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(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

Chen

et al. 2022

Ecological Applications

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Elucidating processes and mechanisms involved in rapid local adaptation to varied environments is a poorly understood but crucial component in management of invasive species. Recent studies have proposed that genetic and epigenetic variation could both contribute to ecological adaptation, yet it remains unclear on the interplay between these two components underpinning rapid adaptation in wild animal populations. To assess their respective contributions to local adaptation, we explored epigenomic and genomic responses to environmental heterogeneity in eight recently colonized ascidian (Ciona intestinalis) populations at a relatively fine geographical scale. Based on MethylRADseq data, we detected strong patterns of local environment‐driven DNA methylation divergence among populations, significant epigenetic isolation by environment (IBE), and a large number of local environment‐associated epigenetic loci. Meanwhile, multiple genetic analyses based on single nucleotide polymorphisms (SNPs) showed genomic footprints of divergent selection. In addition, for five genetically similar populations, we detected significant methylation divergence and local environment‐driven methylation patterns, indicating the strong effects of local environments on epigenetic variation. From a functional perspective, a majority of functional genes, Gene Ontology (GO) terms, and biological pathways were largely specific to one of these two types of variation, suggesting partial independence between epigenetic and genetic adaptation. The methylation quantitative trait loci (mQTL) analysis showed that the genetic variation explained only 18.67% of methylation variation, further confirming the autonomous relationship between these two types of variation. Altogether, we highlight the complementary interplay of genetic and epigenetic variation involved in local adaptation, which may jointly promote populations' rapid adaptive capacity and successful invasions in different environments. The findings here provide valuable insights into interactions between invaders and local environments to allow invasive species to rapidly spread, thus contributing to better prediction of invasion success and development of management strategies.

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Genetic signatures of natural selection in a model invasive ascidian

Cited by 20 publications

References 61 publications

Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins

Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins

Methylation divergence of invasive Ciona ascidians: Significant population structure and local environmental influence

(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

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