Evolutionary consequences of pesticide exposure include transgenerational plasticity and potential terminal investment transgenerational effects

Abstract

Transgenerational plasticity, the influence of the environment experienced by parents on the phenotype and fitness of subsequent generations, is being increasingly recognized. Human-altered environments, such as those resulting from the increasing use of pesticides, may be major drivers of such cross-generational influences, which in turn may have profound evolutionary and ecological repercussions. Most of these consequences are, however, unknown. Whether transgenerational plasticity elicited by pesticide exposure is common, and the consequences of its potential carryover effects on fitness and population dynamics, remains to be determined. Here, we investigate whether exposure of parents to a common pesticide elicits intra-, inter-, and transgenerational responses (in F0, F1, and F2 generations) in life history (fecundity, longevity, and lifetime reproductive success), in an insect model system, the seed beetle Callosobruchus maculatus. We also assessed sex specificity of the effects. We found sex-specific and hormetic intergenerational and transgenerational effects on longevity and lifetime reproductive success, manifested both in the form of maternal and paternal effects. In addition, the transgenerational effects via mothers detected in this study are consistent with a new concept: terminal investment transgenerational effects. Such effects could underlie cross-generational responses to environmental perturbation. Our results indicate that pesticide exposure leads to unanticipated effects on population dynamics and have far-reaching ecological and evolutionary implications.

Pesticide exposure triggers sex-specific inter- and transgenerational effects conditioned by past sexual selection

“…Our results show that there are important and far-reaching transgenerational effects of non-lethal pesticide exposure, as we detected an increase in the longevity of grandsons whose grandparent was exposed, regardless of their sex. These results are consistent with Castano-Sanz et al [38], who showed that grand-offspring lived longer after parental exposure to deltamethrin. Extended longevity implies higher chances for additional matings, and consequently an increased number of descendants.…”

“…These C. maculatus selection lines were raised under either enforced monogamy or unrestricted polygamy for over 84 generations, therefore, imposing relaxed versus strong sexual selection, respectively [43,44]. In a previous study, we confirmed that non-lethal concentrations of the pesticide deltamethrin trigger transgenerational effects in a population of C. maculatus [38]. Here, we exposed males and females from the experimentally evolved lines differing in the strength of sexual selection to the pesticide, hence testing the role of past sexual selection in shaping stress-induced transgenerational effects (figure 1).…”

“…Pesticide exposure triggers detoxification processes in beetles that may result in resource allocation conflicts, which can themselves bear consequences for subsequent generations [96][97][98]. Furthermore, it has been shown that some chemicals, like pesticides, can have hormetic effects triggering responses contrary to expectation when applied at sublethal doses [38,[99][100][101][102]. The application of such toxicants may therefore have unforeseen consequences in subsequent generations and even result, counterintuitively, in population increases [38,42].…”

“…Furthermore, it has been shown that some chemicals, like pesticides, can have hormetic effects triggering responses contrary to expectation when applied at sublethal doses [38,[99][100][101][102]. The application of such toxicants may therefore have unforeseen consequences in subsequent generations and even result, counterintuitively, in population increases [38,42].…”

Parental exposure to heat waves improves offspring reproductive investment in Tetranychus urticae (Acari: Tetranychidae), but not in its predator, Phytoseiulus persimilis (Acari: Phytoseiidae)

“…Nonetheless, most ectothermic females reach adulthood at a smaller size under high temperatures (Angilletta Jr, 2009 ; Atkinson, 1994 ), but there are also exceptions to this temperature–size rule (Fu et al., 2016 ; Kingsolver et al., 2007 ; Walters & Hassall, 2006 ; Walzer et al., 2020 ). Third, in species with sexually dimorphic egg sizes, heat‐stressed females may also invest energy depending on offspring sex, as documented in predatory mites exposed to food stress (Walzer & Schausberger, 2015 ) and seed beetles exposed to pesticides (Castano‐Sanz et al., 2022 ).…”