Acclimation and transgenerational plasticity support increased cadmium tolerance in Gammarus populations exposed to natural metal contamination in headwater streams

Considering long-term population effects of chronic exposure to contaminants remains limited in ecological risk assessment. Field evidence that multigenerational exposure influences organisms' sensitivity is still scarce, and mechanisms have yet to be elucidated in the environmental context. This study focuses on the crustacean Gammarus fossarum, for which an increased tolerance to cadmium (Cd) has previously been reported in a naturally low-contaminated headwater stream. Our objectives were to investigate whether Cd tolerance is a common phenomenon in headwater populations, and to elucidate the nature of the tolerance and its intergenerational transmission. For this, we carried out an in-depth in situ characterization of Cd exposure (gammarids' caging) and levels of tolerance in nine populations on a regional scale, as well as laboratory maintenance and cross-breeding of contaminated and uncontaminated populations. Acute tolerance levels correlate positively with bioavailable Cd contamination levels among streams. The contaminated and non-contaminated populations differ about two-fold in sensitivity to Cd. Tolerance was found in all age classes of contaminated populations, it can be transiently lost during the year, and it was transmissible to offspring. In addition, tolerance levels dropped significantly when organisms were transferred to a Cd-free environment for two months. These organisms also ceased producing tolerant offspring, confirming a non-genetic transmission of Cd tolerance between generations. These findings support that Cd tolerance corresponds to non-genetic acclimation combined with transgenerational plasticity. Moreover, cross-breeding revealed that tolerance transmission to offspring is not limited to maternal effect. We suggest epigenetics as a plausible mechanism for the plasticity of Cd sensitivity observed in the field. Our results therefore highlight the neglected role of plasticity and non-genetic transmission of modified sensitivities during the long-term exposure of natural populations to environmental contamination.

Automated summary

This study investigates the tolerance of the crustacean Gammarus fossarum to cadmium contamination and reveals its characteristics and intergenerational transmission. It is found that the cadmium tolerance of contaminated populations is about two times higher than non-contaminated populations, and this tolerance exists in all age classes of the contaminated populations and can be transmitted to offspring. Additionally, it is observed that the tolerance levels significantly decrease when the organisms are transferred to a cadmium-free environment, and the production of tolerant offspring ceases, confirming the non-genetic transmission of cadmium tolerance. These findings highlight the neglected role of plasticity and non-genetic transmission in the long-term exposure of natural populations to environmental contamination.