Environmental versus anthropogenic effects on population adaptive divergence in the freshwater snail Lymnaea stagnalis

Abstract

Repeated pesticide contaminations of lentic freshwater systems located within agricultural landscapes may affect population evolution in non-target organisms, especially in species with a fully aquatic life cycle and low dispersal ability. The issue of evolutionary impact of pollutants is therefore conceptually important for ecotoxicologists. The impact of historical exposure to pesticides on genetic divergence was investigated in the freshwater gastropod Lymnaea stagnalis, using a set of 14 populations from contrasted environments in terms of pesticide and other anthropogenic pressures. The hypothesis of population adaptive divergence was tested on 11 life-history traits, using Q(ST)-F(ST) comparisons. Despite strong neutral differentiation (mean F(ST) = 0.291), five adult traits or parameters were found to be under divergent selection. Conversely, two early expressed traits showed a pattern consistent with uniform selection or trait canalization, and four adult traits appeared to evolve neutrally. Divergent selection patterns were mostly consistent with a habitat effect, opposing pond to ditch and channel populations. Comparatively, pesticide and other human pressures had little correspondence with evolutionary patterns, despite hatching rate impairment associated with global anthropogenic pressure. Globally, analyses revealed high genetic variation both at neutral markers and fitness-related traits in a species used as model in ecotoxicology, providing empirical support for the need to account for genetic and evolutionary components of population response in ecological risk assessment.

Figure 1. Location of 14 L. stagnalis populations involved in Q _ST-F _ST comparisons.

Populations are coded from 1 to 14. Colours indicate environmental categories (white, grey, and black, for GEP, GEP1, and GEP2, respectively). See Table 1 for details.

Figure 2. Schematic overview of the common garden experiment used to investigate population divergence in L. stagnalis.

Figure 3. Population genetic differentiation in L. stagnalis.

(A) Bayesian assignment probabilities in Structure analysis, for k = 2 clusters. Each bar represents an individual. Bar colour indicates the posterior probability that the individual belongs to the cluster of that color. (B) Unrooted Neighbour-Joining tree based on population pairwise F _ST values (see Table S4).

Figure 4. Correlation plot between 14-days fecundity and (A) population expected heterozygosity, (B) population inbreeding, as based on 14 L. stagnalis populations.