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.

Highlights

  • Understanding the causes of genetic divergence within species is a central goal in evolutionary biology

  • Populations were classified according to four criteria: habitat (H: pond, channel, ditch), pesticide pressure (PP: two levels, low vs high), other anthropogenic pressure (OAP: two levels, low vs high), and global environmental pressure, as a combination of pesticide and other anthropogenic pressures (GEP: three levels)

  • Effective population size Ne was significantly larger in sites exposed to high pesticide pressure

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Summary

Introduction

Understanding the causes of genetic divergence within species is a central goal in evolutionary biology. Evolutionary change can be rapid, especially in the current environmental context. Besides evolutionary textbook cases of insecticide resistance [4], environmental stress may trigger fast evolutionary responses [5], and rapid adaptive responses have been documented in ecological situations involving anthropogenic disturbance [6,7]. It is noteworthy that the rate of phenotypic change can itself increase in human-disturbed and toxic environments [8,9]. The potential evolutionary impact of chemicals and toxic substances released by human activities into the environment is still not considered in current procedures of ecological risk assessment. Beyond mutagenic compounds affecting the germline, pollutants have proved to be potential sources of evolutionary impact, as supported empirically by an ever growing number of studies [15,16,17,18,19,20,21,22,23]

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