Whole-genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

Abstract

The sympatric existence of genetically distinct populations of the same species remains a puzzle in ecology. Coexisting salmonid fish populations are known from over 100 freshwater lakes. Most studies of sympatric populations have used limited numbers of genetic markers making it unclear if genetic divergence involves only certain parts of the genome. We return to the first reported case of salmonid sympatry, initially detected through contrasting homozygosity at a single allozyme locus (lactate dehydrogenase, LDH-A1) in brown trout in the small Lakes Bunnersjöarna, central Sweden. We use DNA from samples collected in the 1970s and a 96 SNP fluidigm array to verify the existence of the coexisting demes. We then apply whole-genome resequencing of pooled DNA to explore genome-wide diversity within and between these demes; strong genetic divergence is observed with genome-wide FST=0.13. Nucleotide diversity is estimated to 0.0013 in Deme I but only 0.0005 in Deme II. Individual whole-genome resequencing of two individuals per deme suggests considerably higher inbreeding in Deme II vs. Deme I. Comparing with similar data from other lakes we find that the genome-wide divergence between the demes is similar to that between reproductively isolated populations. We located two genes for LDH-A and found divergence between the demes in a regulatory section of one of the genes, but we could not find a perfect fit between allozyme and sequence data. Our data demonstrate genome-wide divergence governed by genetic drift and diversifying selection, confirming reproductive isolation between the sympatric demes.

Genomic dynamics of brown trout populations released to a novel environment

“…Generally, presently estimated population metrics appear low in comparison to observations from other wild salmonid populations (Leitwein et al, 2016; Willoughby et al, 2018). However, our own studies of natural brown trout in nearby mountain lake systems (ecologically similar to the system studied here), using a variety of genetic markers, indicate that the diversity levels of the established populations LB and HV are among the highest observed (Andersson et al, 2017; Kurland et al, 2019; Palm et al, 2003; Palmé et al, 2013; Saha et al, 2022). It is interesting to note that even though the established population HV is located several kilometers away from the release site, genetic diversity is highest here.…”

“…Population differentiation was estimated using F ST from the “fst‐sliding.pl” script in PoPoolation2 v.2.2 (Kofler, Pandey, et al, 2011) within non‐overlapping windows of 5 kb to minimize stochastic errors linked to small window sizes (Kofler, Pandey, et al, 2011; Saha et al, 2022). F ST was estimated using the default, Nei's (1973), approach, as well as one provided by Karlsson et al (2007), which is expected to return estimates more in line with those from individually genotyped SNPs (i.e., Weir & Cockerham, 1984; cf.…”

“…For polyploid species, for example, the brown trout, paralogous regions are expected to have high coverage. In order to eliminate artefactual results caused by coverage fluctuations, the mpileup was subsampled based on the mode of the read depth histogram for each pool, to 20–150× using the “subsample‐pileup.pl” script implemented in PoPoolation v.2.2 (Kofler, Orozco‐terWengel, et al, 2011) in accordance with best practices for polyploid species (Micheletti et al, 2018; Narum et al, 2013) and as previously conducted for brown trout (Kurland et al, 2019; Saha et al, 2022). Additional details on quality assessment, window sizes, quality filtering, and parameter settings are described in Appendix .…”

“…F ST was estimated using the default, Nei's (1973), approach, as well as one provided by Karlsson et al (2007), which is expected to return estimates more in line with those from individually genotyped SNPs (i.e., Weir & Cockerham, 1984; cf. Saha et al, 2022, their Appendix S4).…”

Genomic survey of edible cockle (Cerastoderma edule) in the Northeast Atlantic: A baseline for sustainable management of its wild resources

“…current systems, fronts, gyres and eddies) or environmental gaps limiting dispersal (Blanco‐González et al, 2016; Nielsen et al, 2004; Vera et al, 2016; Xuereb et al, 2018), but also natural local selection in response to environmental variation (Clucas et al, 2019; Jiménez‐Mena et al, 2020; Vilas et al, 2015). Furthermore, historical vicariance, not yet erased by gene flow, and reproductive isolation can be other factors explaining differentiation (Gagnaire et al, 2015; Riginos et al, 2016; Saha et al, 2021). Distinguishing between neutral and adaptive genetic variation in the marine landscape has become a central issue in conservation biology, allowing for interpreting genetic variation in both historical/demographic and adaptive terms (Bernatchez, 2016; Nielsen et al, 2009).…”