RAD-Seq Reveals Patterns of Additive Polygenic Variation Caused by Spatially-Varying Selection in the American Eel (Anguilla rostrata)

Abstract

The American Eel (Anguilla rostrata) has an exceptional life cycle characterized by panmictic reproduction at the species scale, random dispersal, and selection in a highly heterogeneous habitat extending from subtropical to subarctic latitudes. The genetic consequences of spatially-varying selection in this species have been investigated for decades, revealing subtle clines in allele frequency at a few loci that contrast with complete panmixia on the vast majority of the genome. Because reproduction homogenizes allele frequencies every generation, sampling size, and genomic coverage are critical to reach sufficient power to detect selected loci in this context. Here, we used a total of 710 individuals from 12 sites and 12,098 high-quality single nucleotide polymorphisms to re-evaluate the extent to which local selection affects the spatial distribution of genetic diversity in this species. We used environmental association methods to identify markers under spatially-varying selection, which indicated that selection affects ∼1.5% of the genome. We then evaluated the extent to which candidate markers collectively vary with environmental factors using additive polygenic scores. We found significant correlations between polygenic scores and latitude, longitude and temperature which are consistent with polygenic selection acting against maladapted genotypes in different habitats occupied by eels throughout their range of distribution. Gene functions associated with outlier markers were significantly enriched for the insulin signaling pathway, indicating that the trade-offs inherent to occupying such a large distribution range involve the regulation of metabolism. Overall, this study highlights the potential of the additive polygenic scores approach in detecting selective effects in a complex environment.

Local and regional scale habitat heterogeneity contribute to genetic adaptation in a commercially important marine mollusc (Haliotis rubra) from southeastern Australia

“…Specifically, our genotype‐environmental association analyses suggest genotype associations with habitat features such as local reef geology, reef complexity, and exposure to wave power and ocean currents that vary over scales of tens to hundreds of metres (Ierodiaconou et al, ; Young et al, ). Evidence of finescale adaptive genetic structuring is unusual in dispersive marine species, with a few exceptions (Babin, Gagnaire, Pavey, & Bernatchez, ; Sherman & Ayre, ). While we cannot completely rule out the influence of false positives, each genotype‐environment association (GEA) detected was corrected for spatial structure and distance, and our sampling regime contrasted genetic variation across distinct habitat types present both within and between western, central, and eastern regions of the state.…”

“…This is not a novel finding; evidence of phenotype‐environment mismatches impacting recruitment dynamics and reducing population connectivity in dispersive marine species is well documented and summarised in Marshall et al (). Natural selection could potentially occur at pre‐ or post‐settlement stages in H. rubra, as seen in other marine and diadromous taxa (Babin et al, ; Sherman & Ayre, ). In some marine species, environmental cues influence the settlement of larvae from the water column (Harrington, Fabricius, De'ath, & Negri, ; Rodriguez, Ojeda, & Inestrosa, ; Sneed, Sharp, Ritchie, & Paul, ), with encrusting coralline algae, macroalgae, and mucus trails reported to be potential settlement cues for Haliotids (Huggett, de Nys, Williamson, Heasman, & Steinberg, ; Morse, Froyd, & Morse, ; Takami, Kawamura, & Yamashita, ).…”

Seascape genomics of eastern oyster (Crassostrea virginica) along the Atlantic coast of Canada

“…As a final step for the multilocus approach, we calculated a polygenic score to assess the individual cumulative adaptive genetic variation associated with each environmental variable tested (Babin, Gagnaire, Pavey, & Bernatchez, 2017;Gagnaire & Gaggiotti, 2016).…”

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

“…Evidence of local adaptation associated with environmental conditions in marine populations is growing, challenging the dogma that a high degree of gene flow precludes adaptive divergence in the ocean (Bernatchez, ; Sanford & Kelly, ). Empirical studies have identified key environmental predictors of adaptive genetic variation across environmental gradients in marine taxa including corals (Lundgren, Vera, Peplow, Manel, & van Oppen, ), eels (Babin, Gagnaire, Pavey, & Bernatchez, ; Gagnaire et al, ), sticklebacks (Guo, DeFaveri, Sotelo, Nair, & Merilä, ), lobsters (Benestan et al, ), and Pacific (Hecht, Matala, Hess, & Narum, ) and Atlantic (Jeffery et al, ) salmon.…”