Small-scale population structuring results in differential susceptibility to pesticide exposure

Abstract

Central European riverine networks are subject to widely varying local anthropogenic pressures, forcing species with limited dispersal abilities to adapt or become locally extinct. Previous catchment-wide studies have shown that some invertebrates tend to have pronounced population structuring throughout mountainous river networks, raising the question of whether this also translates into small-scale phenotypic differentiation and adaptation to local stressors. One such species is the headwater crustacean species Gammarus fossarum clade 11 (or lineage B), which we restudied in terms of population structure four years after first assessment. Our aim was not only to document the temporal stability/dynamics of the population structure, but we asked whether a small-scale genetic structuring also results in phenotypic differentiation and different susceptibility to a commonly applied pesticide. Therefore, we re-assessed population structure based on COI haplotypes and their frequencies, and quantified key parameters related to morphological and life-history differentiation. Furthermore, we examined the difference in sensitivity towards the pyrethroid insecticide deltamethrin. COI haplotype patterns were found to be stable over time and confirmed the small-scale population structuring within the catchment, with isolated headwater populations and connected downstream populations. While little life-history differentiation was observed, marked differences in susceptibility to the pyrethroid insecticide were found. Populations from pristine sites responded significantly more tolerant than populations from anthropogenically impacted sites—showing that prior exposure to a spectrum of stressors does not automatically increase tolerance to a specific stressor. Therefore, our study demonstrates that limited dispersal capacity is reflected not only in population structure, but also in small-scale variation in susceptibility to anthropogenic disturbance. The system thus provides a suitable experimental landscape to test the impact of further stressors (e.g., other novel entities, including pesticides with other modes of action) on locally isolated populations. Based on these findings, important recommendations for the protection of riverine species and their intraspecific genetic variation can be developed.

Infection with acanthocephalans increases tolerance of Gammarus roeselii (Crustacea: Amphipoda) to pyrethroid insecticide deltamethrin

“…Lethal limits were reported for G. fossarum and G. pulex , with a 96-h LC 50 of 33.2 and 68.0 ng/l, respectively (Adam et al 2010 ). However, some variability in the response to deltamethrin was reported for populations of Gammarus sp., suggesting potential adaptations to the stressor in some populations (Adam et al 2010 ; Grethlein et al 2022 ). Our study complements these findings and shows that there may be differences in sensitivity not only between populations of the same species, but even within a population, depending on acanthocephalan infections.…”

“…These effects manifest as incoordination, convulsions, and paralysis of the organism (Soderlund and Bloomquist 1989 ; Davies et al 2007 ). Deltamethrin has been shown to be toxic to Gammarus even at very low concentrations (Adam et al 2010 ; Grethlein et al 2022 ) which motivated us to choose it as a model toxicant.…”

Cryptic Species in Ecotoxicology

“…Our examples show that some cryptic species may have evolved unique adaptations that make them more resilient to pollutants, despite their phylogenetic relationships with more vulnerable species of the cryptic species complex (see Monteiro et al, 2018;Rocha-Olivares et al, 2004;Weston et al, 2013). Therefore, although phylogenetic similarity may provide some clues about vulnerability to pollutants, it is not always a reliable predictor and must be considered in the light of individual evolutionary history and possible points of contact with stressors (Best & Stachowicz, 2013;Grethlein et al, 2022). Therefore conservationists and policymakers should consider this complexity when making informed decisions on species diversity and distribution.…”

“…If both species are transferred to a common stock (i.e., pooled), the tolerance of both species is taken into account, which increases the variance and might blur the overall results (Figure 1C). (2) The variance in species-specific susceptibility (i.e., population-specific differentiation; Grethlein et al, 2022) may differ significantly, resulting in a wider range of tolerance (Figure 1E). If the species with high variance is considered (Figure 1F), the species with low variance is covered.…”

“…Populations can differ significantly, sometimes over small geographic distances, and the effect can be reinforced by laboratory inbreeding. Adaptive processes have repeatedly been identified in chronically exposed populations, in which concentration-response patterns have differed across populations, which can be explained by microevolutionary processes (see Barata et al, 2002;Grethlein et al, 2022;Jourdan et al, 2019;Morgan et al, 2007;Shahid et al, 2018;Weston et al, 2013). In contrast, cryptic species usually represent much older evolutionary splits and thus reflect macro-evolutionary processes.…”