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Genomic consequences of human-mediated translocations in margin populations of an endangered amphibian.

ABSTRACT: Due to their isolated and often fragmented nature, range margin populations are especially vulnerable to rapid environmental change. To maintain genetic diversity and adaptive potential, gene flow from disjunct populations might therefore be crucial to their survival. Translocations are often proposed as a mitigation strategy to increase genetic diversity in threatened populations. However, this also includes the risk of losing locally adapted alleles through genetic swamping. Human-mediated translocations of southern lineage specimens into northern German populations of the endangered European fire-bellied toad (Bombina bombina) provide an unexpected experimental set-up to test the genetic consequences of an intraspecific introgression from central population individuals into populations at the species range margin. Here, we utilize complete mitochondrial genomes and transcriptome nuclear data to reveal the full genetic extent of this translocation and the consequences it may have for these populations. We uncover signs of introgression in four out of the five northern populations investigated, including a number of introgressed alleles ubiquitous in all recipient populations, suggesting a possible adaptive advantage. Introgressed alleles dominate at the MTCH2 locus, associated with obesity/fat tissue in humans, and the DSP locus, essential for the proper development of epidermal skin in amphibians. Furthermore, we found loci where local alleles were retained in the introgressed populations, suggesting their relevance for local adaptation. Finally, comparisons of genetic diversity between introgressed and nonintrogressed northern German populations revealed an increase in genetic diversity in all German individuals belonging to introgressed populations, supporting the idea of a beneficial transfer of genetic variation from Austria into North Germany.

SUBMITTER: De Cahsan B

PROVIDER: S-EPMC8210794 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Coldwater-adapted freshwater fishes, especially their populations along warm-range margins, are most vulnerable to the climate oscillations associated with global warming. Stocking is a major strategy for avoiding the extinction of these species. However, while stocking can reverse the decline of isolated populations, it may also result in a loss of genetic diversity in the native local population due to the introgressive replacement of hatchery genes. To plan an adequate strategy for conserving locally adapted populations, the genetic impacts of stocking on native lineages should be evaluated from small river branches to wide-ranging drainage areas. We investigated the population genetic structure of white-spotted charr (Salvelinus leucomaenis) within its southern range (Lake Biwa basin, Japan). By applying genome-wide SNP analysis to the population's genetic structure, we assessed the extent of genetic introgression resulting from stocking. White-spotted charr in the Lake Biwa watershed constitutes a distinctive genetic group, within which apparent genetic differentiation was observed. The hatchery-reared fish line commonly used for supplementation stocking in the catchment was discernable from the native population, enabling us to analyze genetic introgression across the entire drainage area. Admixed individuals resulting from hatchery introgression were observed in most of the stocked sites that showed relatively high heterozygosity and nucleotide diversity. However, their genetic differentiation was much lower than that of native populations. The supplementation history as well as the road availability contributed substantially to the introgression of hatchery genes. Populations with the native genetic structure remained in the upstream regions of the tested rivers. However, their heterozygosity and nucleotide diversity were low when compared with that of the populations with hatchery supplementation. Our results shed light on the genetic impacts of stocking on isolated native populations and suggest that conventional supplementation methods cannot preserve a unique biodiversity in the distribution margin.

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Genomic consequences of human-mediated translocations in margin populations of an endangered amphibian.

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