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

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 (coding for
lactate dehydrogenase A) in brown trout in the small Lakes Bunnersjöarna,
Sweden. First, we verify the existence of the two coexisting demes using a
96-SNP fluidigm array. We then apply whole-genome resequencing of pooled
DNA to explore genome-wide diversity within and between these demes;
nucleotide diversity is higher in Deme I than in Deme II. Furthermore,
strong genetic divergence is observed with genome-wide FST≈0.2. Comparing
with similar data from other lakes, this divergence is of similar
magnitude as that between reproductively isolated populations. Individual
whole-genome resequencing of two individuals per deme suggests higher
inbreeding in Deme II vs. Deme I, indicating different degree of
isolation. Finally, we located two gene-copies for LDH-A and find
divergence between demes in a regulatory section of one of these genes.
However, we did not find a perfect fit between the sequence data and
previous allozyme results, and this will require further research. Our
data demonstrates genome-wide divergence governed mostly by genetic drift
but also by diversifying selection in coexisting populations. This type of
hidden biodiversity needs consideration in conservation management.