Genetic diversity is the basis for population adaptation and long-term survival, yet rarely considered in biodiversity monitoring. One key issue is the need for useful and straightforward indicators of genetic diversity. To test newly proposed indicators, we monitored genetic diversity over 40 years (1970-2010) in metapopulations of brown trout inhabiting 27 small mountain lakes representing 10 water systems in central Sweden. Three of the indicators were previously proposed for broad, international use for the Convention on Biological Diversity (CBD) context, while three others were recently elaborated for national use by a Swedish science-management effort and applied for the first time here. The Swedish indicators use molecular genetic data to monitor genetic diversity within and between populations and assess the effective population size (Ne). We used a panel of 96 SNPs and identified 29 discrete populations retained over time. Over 40 percent of the lakes harbored more than one population indicating that brown trout biodiversity hidden as cryptic, sympatric populations are more common than recognized. The Ne indicator showed values below the threshold (Ne≤500) in 20 populations with five showing Ne<100. Although statistically significant genetic diversity reductions occurred in several populations, they were mostly within proposed threshold limits. Metapopulation structure appears to buffer against diversity loss; when applying the indicators to metapopulations most indicators suggest an acceptable genetic status in all but one system. The CBD indicators agreed with the national ones but provided less detail. We propose that all indicators applied here are appropriate for monitoring genetic diversity within species.

Understanding the consequences of human induced translocations on natural populations requires genetic monitoring. Salmonid fishes represent a group of species experiencing several such large-scale perturbations expected to affect microevolutionary processes. Here, two genetically separate brown trout populations with divergent life history traits are studied following their release into waters previously void of trout. We use a pooled sequencing approach to explore the genomic characteristics of the released stocks and of populations established in the wild in two lakes down-stream of the release site 30 years (4-5 generations) later. While most of the differences (FST=0.16) between the released stocks can be attributed to drift, we identify putatively adaptive differences between them in genes involved in immunity, hearing, skin and muscle texture. Higher levels of genome-wide diversity in established populations compared to released stocks suggest extensive hybridization between stocks. However, released stocks are unequally represented in the established populations, with one stock mainly contributing to the lake closest to the release site, and the other dominating the lake further downstream. We also identify genomic regions putatively under directional selection in the new environment, where genes from one of the released populations, governing metabolism, appear advantageous. Our results demonstrate that hybridization, establishment, and adaptation can be rapid after release into novel environments. We show that such ongoing processes, important for conservation and management, are possible to monitor over contemporary time scales even for a species with relatively small local effective population sizes and a large, complex genome.

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.