AFLPs and mitochondrial haplotypes reveal local adaptation to extreme thermal environments in a freshwater gastropod

Abstract

The way environmental variation shapes neutral and adaptive genetic variation in natural populations is a key issue in evolutionary biology. Genome scans allow the identification of the genetic basis of local adaptation without previous knowledge of genetic variation or traits under selection. Candidate loci for divergent adaptation are expected to show higher FST than neutral loci influenced solely by random genetic drift, migration and mutation. The comparison of spatial patterns of neutral markers and loci under selection may help disentangle the effects of gene flow, genetic drift and selection among populations living in contrasting environments. Using the gastropod Radix balthica as a system, we analyzed 376 AFLP markers and 25 mtDNA COI haplotypes for candidate loci and associations with local adaptation among contrasting thermal environments in Lake Mývatn, a volcanic lake in northern Iceland. We found that 2% of the analysed AFLP markers were under directional selection and 12% of the mitochondrial haplotypes correlated with differing thermal habitats. The genetic networks were concordant for AFLP markers and mitochondrial haplotypes, depicting distinct topologies at neutral and candidate loci. Neutral topologies were characterized by intense gene flow revealed by dense nets with edges connecting contrasting thermal habitats, whereas the connections at candidate loci were mostly restricted to populations within each thermal habitat and the number of edges decreased with temperature. Our results suggest microgeographic adaptation within Lake Mývatn and highlight the utility of genome scans in detecting adaptive divergence.

Figure 1. Map of Lake Mývatn (Iceland) showing the localization of the area of study (water body colored).

Circles depict sites at high temperature (24°C); triangles show sites at intermediate temperatures (12–19°C), and squares correspond to sites at low temperature (6–8°C). See the text for further information.

Figure 2. Hierarchical Bayesian clustering for the six populations genotyped at 117 neutral loci.

First (upper barplot, Fig. 2A), inferred ancestry of individuals was calculated after averaging ten STRUCTURE – runs with CLUMPP . The number of clusters that best fits the total data was K = 2 after Evanno's correction (ΔK = 306). Then (lower barplots, Fig. 2B), the same procedure was performed again for every cluster obtaining K = 3 for each of the subsets (ΔK = 58 and ΔK = 242 for high and low temperature respectively). Sites are ordered in the barplots according to the N-S directions that corresponds to decreasing habitat temperatures.

Figure 3. Graphs of the genetic networks for AFLPs (upper row) and COI (lower row).

Nuclear networks have been created with: a) eight loci under stabilizing selection, b) 117 neutral loci and c) four loci under directional selection; whereas mitochondrial networks have been created with d) 22 uncorrelated haplotypes and e) three haplotypes associated with temperature. Black circles represent populations in high temperature sites (24°C), grey circles depict intermediate temperatures (12–19°C) and white circles represent sites at low temperature (6–8°C). Site pairs in a network connected by lines are considered to exchange migrants exhibiting significant conditional genetic covariance. Solid lines indicate connections assuming an IBD process where genetic distances and spatial distances are proportional. Dotted lines (…) represent compressed edges with relatively higher conditional genetic distance (cGD) in respect to spatial distance (suggesting geographical or ecological barriers), whereas dashed lines (---) depict extended edges indicating long distance migration processes.