Rapid adaptation through genomic and epigenomic responses following translocations in an endangered salmonid.

Alex A Lyle,Colin E Adams,Kathryn R Elmer,Elizabeth Yohannes,Ian J Winfield,Marco Crotti

doi:10.1111/eva.13267

Abstract

Identifying the molecular mechanisms facilitating adaptation to new environments is a key question in evolutionary biology, especially in the face of current rapid and human‐induced changes. Translocations have become an important tool for species conservation, but the attendant small population sizes and new ecological pressures might affect phenotypic and genotypic variation and trajectories dramatically and in unknown ways. In Scotland, the European whitefish (Coregonus lavaretus) is native to only two lakes and vulnerable to extirpation. Six new refuge populations were established over the last 30 years as a conservation measure. In this study, we examined whether there is a predictable ecological and evolutionary response of these fishes to translocation. We found eco‐morphological differences, as functional traits relating to body shape differed between source and refuge populations. Dual isotopic analyses suggested some ecological release, with the diets in refuge populations being more diverse than in source populations. Analyses of up to 9117 genome‐mapped SNPs showed that refuge populations had reduced genetic diversity and elevated inbreeding and relatedness relative to source populations, though genomic differentiation was low (F ST = 0.002–0.030). We identified 14 genomic SNPs that showed shared signals of a selective response to translocations, including some located near or within genes involved in the immune system, nervous system and hepatic functions. Analysis of up to 120,897 epigenomic loci identified a component of consistent differential methylation between source and refuge populations. We found that epigenomic variation and genomic variation were associated with morphological variation, but we were not able to infer an effect of population age because the patterns were also linked with the methodology of the translocations. These results show that conservation‐driven translocations affect evolutionary potential by impacting eco‐morphological, genomic and epigenomic components of diversity, shedding light on acclimation and adaptation process in these contexts.

Highlights

Conservation-driven translocations are the intentional, human- mediated movement and release of an organism outside its recorded range, with the aim of establishing new populations to mitigate against the extinction of important conservation units (IUCN & SCC, 2013)
We found five genes putatively under differential selection in refuge populations compared with source and that might be involved in local adaptation to the new environments
Future high-d ensity genome-wide research of methylation would be valuable for inferring functional targets and responses across translocation environments. This effect is evident in our finding that lake type explained substantially more variance in the epigenomic models than it did in the genomic models (35% vs 3% of the variance captured in the redundancy analysis (RDA))

Summary

Introduction

Conservation-driven translocations are the intentional, human- mediated movement and release of an organism outside its recorded range, with the aim of establishing new populations to mitigate against the extinction of important conservation units (IUCN & SCC, 2013). Population-level consequences of translocations are expected but the ecological and evolutionary responses poorly understood. Refuge populations experience differential selection due to novel environmental pressures and in some cases have shown rapid genomic adaptation within the first few generations of a translocation (Laurentino et al, 2020; Marques et al, 2018). Unlike natural range expansions or new colonizations by dispersing individuals, the human influence on conservation translocations and the already at-risk status of the populations are expected to have genomic consequences on the evolutionary trajectories that are difficult to predict

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