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

Auréline Lalouette; Davide Degli Esposti; Laura Garnero; Maxime Allibert; Lysiane Dherret; Aymeric Dabrin; Nicolas Delorme; Rémi Recoura-Massaquant; Arnaud Chaumot

doi:10.1016/j.scitotenv.2023.166216

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

Sci Total Environ. 2023 Dec 10:903:166216. doi: 10.1016/j.scitotenv.2023.166216. Epub 2023 Aug 9.

Authors

Auréline Lalouette¹, Davide Degli Esposti¹, Laura Garnero¹, Maxime Allibert¹, Lysiane Dherret², Aymeric Dabrin², Nicolas Delorme¹, Rémi Recoura-Massaquant¹, Arnaud Chaumot³

Affiliations

¹ INRAE, UR RiverLy, Laboratoire d'écotoxicologie, Villeurbanne F-69625, France.
² INRAE, UR RiverLy, Laboratoire de chimie des milieux aquatiques, Villeurbanne F-69625, France.
³ INRAE, UR RiverLy, Laboratoire d'écotoxicologie, Villeurbanne F-69625, France. Electronic address: arnaud.chaumot@inrae.fr.

PMID: 37567286
DOI: 10.1016/j.scitotenv.2023.166216

Abstract

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.

Keywords: Adaptation; Amphipods; Evolution; Multigenerational exposure; Non-genetic transmission; Parental effect.