Putatively adaptive genetic variation in the giant California sea cucumber (Parastichopus californicus) as revealed by environmental association analysis of restriction‐site associated DNA sequencing data

Abstract

Understanding the spatial scale of local adaptation and the factors associated with adaptive diversity are important objectives for ecology and evolutionary biology, and have significant implications for effective conservation and management of wild populations and natural resources. In this study, we used an environmental association analysis to identify important bioclimatic variables correlated with putatively adaptive genetic variation in a benthic marine invertebrate-the giant California sea cucumber (Parastichopus californicus)-spanning coastal British Columbia and southeastern Alaska. We used a redundancy analysis (RDA) with 3,699 single nucleotide polymorphisms (SNPs) obtained using RAD sequencing to detect candidate markers associated with 11 bioclimatic variables, including sea bottom and surface conditions, across two spatial scales (entire study area and within subregions). At the broadest scale, RDA revealed 59 candidate SNPs, 86% of which were associated with mean bottom temperature. Similar patterns were identified when population structure was accounted for. Additive polygenic scores, which provide a measure of the cumulative signal across all candidate SNPs, were strongly correlated with mean bottom temperature, consistent with spatially varying selection across a thermal gradient. At a finer scale, 23 candidate SNPs were detected, primarily associated with surface salinity (26%) and bottom current velocity (17%). Our findings suggest that environmental variables may play a role as drivers of spatially varying selection for P. californicus. These results provide context for future studies to evaluate the genetic basis of local adaptation in P. californicus and help inform the relevant scales and environmental variables for in situ field studies of putative adaptive variation in marine invertebrates. K E Y W O R D S climate data, environmental association analysis, marine invertebrate, RAD-sequencing, redundancy analysis, seascape genomics

Standing genetic variation and chromosomal rearrangements facilitate local adaptation in a marine fish

“…To date, empirical work focusing on the contribution of genomic background (e.g., standing genetic variation and chromosomal rearrangement) to adaptive variation in the presence of high gene flow have been limited to a restricted number of study systems (e.g., Tine et al 2014, Bernatchez 2016, Le Moan et al 2019, Barth et al 2017, Petterson et al 2019. Marine organisms are excellent biological models to address this issue since many marine species experience highly heterogeneous marine conditions potentially acting as selective agents, yet displaying very weak genetic differentiation due to large ܰ and high connectivity associated with strong dispersal capacities (Palumbi 1992, Bradbury et al 2008, Selkoe et al 2016, Xuereb et al 2018. Capelin (Mallotus villosus) is a key-forage fish species (Buren et al 2014) that display such characteristics typical of marine organisms.…”

Multi-model seascape genomics identifies distinct environmental drivers of selection among sympatric marine species

“…Salinity emerging as a major selective force on C. punctatus is understandable, as this species is an osmoconformer that inhabits estuarine environments [64], and because the larval development of decapods is in uenced by changes in salinity [65]. The lack of clear correlations with any environmental variables is unexpected for the urchin P. angulosus, given that previous studies have shown genomic variation corresponding to SST gradients in other echinoderms [28,66]. Additionally, the paucity of annotated genomes for marine invertebrates makes it di cult to identify the functionality of outlier loci, which likely led to the limited number of BLAST hits for the 2X outliers in each species (Additional File 4).…”

“…3). Previous seascape genomic studies in temperate regions have frequently identi ed some measure of SST as the best predictor of genomic variation of marine invertebrates [9,11,12,25,28,63], which is most likely due to SST affecting both cellular processes, and life-history events such as spawning and larval development [59]. However, for P. angulosus, Trange and SSTmean best explained genomic variation, whereas SSSmean best explained the structure of C. punctatus.…”

“…GEAAs are powerful tools to detect putative adaptive loci (commonly termed 'outlier loci') by directly associating allele frequencies with environmental variables [5,23,24]. Sea surface temperature (SST) is the most common environmental structuring force identi ed among seascape studies to date [25], and has been shown to strongly correlate with genomic variation in abalone [14], mussels [26], oysters [12,27], sea cucumbers [28], and lobsters [11]. As SST is consistently identi ed as one of the prominent drivers of genomic variation in marine invertebrates, it has promise as a proxy for evolutionary processes, such as local selection, in conservation [29].…”

Explaining genetic patterns in the Philippines: broad and fine scale perspectives

“…Indeed, a recent genomic study on the summer flounder Paralichthys dentatus found very weak spatial genetic structuring and identified loci whose allele frequency distribution was concordant with temperaturesuggesting adaptive genetic diversity driven by temperature (Hoey & Pinsky, 2018). Similarly, temperature is also suggested to be a driver of adaptive diversity in sea cucumber Parastichopus californicus after statistically controlling for population structuring (Xuereb et al, 2018). With the increasing human-mediated threats to marine biodiversity Urban, 2015), understanding adaptive evolutionary processes is becoming more timely, especially in tropical marine systems that are predicted to be highly impacted by changes in climatic conditions (Molinos et al, 2016).…”