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Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish.

ABSTRACT: The global rise of pharmaceutical contaminants in the aquatic environment poses a serious threat to ecological and evolutionary processes. Studies have traditionally focused on the collateral (average) effects of psychoactive pollutants on ecologically relevant behaviors of wildlife, often neglecting effects among and within individuals, and whether they differ between males and females. We tested whether psychoactive pollutants have sex-specific effects on behavioral individuality and plasticity in guppies (Poecilia reticulata), a freshwater species that inhabits contaminated waterways in the wild. Fish were exposed to fluoxetine (Prozac) for 2 years across multiple generations before their activity and stress-related behavior were repeatedly assayed. Using a Bayesian statistical approach that partitions the effects among and within individuals, we found that males-but not females-in fluoxetine-exposed populations differed less from each other in their behavior (lower behavioral individuality) than unexposed males. In sharp contrast, effects on behavioral plasticity were observed in females-but not in males-whereby exposure to even low levels of fluoxetine resulted in a substantial decrease (activity) and increase (freezing behavior) in the behavioral plasticity of females. Our evidence reveals that psychoactive pollution has sex-specific effects on the individual behavior of fish, suggesting that males and females might not be equally vulnerable to global pollutants.

SUBMITTER: Polverino G

PROVIDER: S-EPMC10636733 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish.

Polverino Giovanni G Aich Upama U Brand Jack A JA Bertram Michael G MG Martin Jake M JM Tan Hung H Soman Vrishin R VR Mason Rachel T RT Wong Bob B M BBM

Behavioral ecology : official journal of the International Society for Behavioral Ecology 20230814 6

The global rise of pharmaceutical contaminants in the aquatic environment poses a serious threat to ecological and evolutionary processes. Studies have traditionally focused on the collateral (average) effects of psychoactive pollutants on ecologically relevant behaviors of wildlife, often neglecting effects among and within individuals, and whether they differ between males and females. We tested whether psychoactive pollutants have sex-specific effects on behavioral individuality and plasticit ...[more]

PMID: 37969553

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Project description:Transgenerational plasticity (TGP) occurs when the environment encountered by one generation (F0) alters the phenotypes of one or more future generations (e.g. F1 and F2). Sex selective TGP, via specific lineages or to only male or female descendants, has been underexplored in natural systems, and may be adaptive if it allows past generations to fine-tune the phenotypes of future generations in response to sex-specific life-history strategies. We sought to understand if exposing males to predation risk can influence grandoffspring via sperm in three-spined stickleback Gasterosteus aculeatus. We specifically tested the hypothesis that grandparental effects are transmitted in a sex-specific way down the male lineage, from paternal grandfathers to F2 males. We reared F1 offspring of unexposed and predator-exposed F0 males under 'control' conditions and used them to generate F2s with control grandfathers, a predator-exposed maternal grandfather (i.e. predator-exposed F0 males to F1 daughters to F2s), a predator-exposed paternal grandfather (i.e. predator-exposed F0 males to F1 sons to F2s) or two predator-exposed grandfathers. We then assayed male and female F2s for a variety of traits related to antipredator defence. We found little evidence that transgenerational effects were mediated to only male descendants via the paternal lineage. Instead, grandpaternal effects depended on lineage and were mediated largely across sexes, from F1 males to F2 females and from F1 females to F2 males. When their paternal grandfather was exposed to predation risk, female F2s were heavier and showed a reduced change in behaviour in response to a simulated predator attack relative to grandoffspring of control, unexposed grandparents. In contrast, male F2s showed reduced antipredator behaviour when their maternal grandfather was exposed to predation risk. However, these patterns were only evident when one grandfather, but not both grandfathers, was exposed to predation risk, suggesting the potential for non-additive interactions across lineages. If sex-specific and lineage effects are common, then grandparental effects are likely underestimated in the literature. These results draw attention to the importance of sex-selective inheritance of environmental effects and raise new questions about the proximate and ultimate causes of selective transmission across generations.

Project description:Chronic social isolation stress (SIS) induces lasting negative effects on the brain, including memory deficits, cognitive impairments, and mood alterations such as depression and anxiety. All these symptoms, at least in part, reflect reduced hippocampal function. In both clinical and preclinical studies, subanesthetic doses of the NMDA receptor antagonist, ketamine (KET), was shown to have rapid and lasting antidepressant effects. Animal studies have shown that biological sex and levels of gonadal hormones alter the behavioral effects of KET, with ovarian hormones increasing sensitivity to the antidepressant-like effects of KET. Since the hippocampus plays a key role in mediating some of the effects of SIS, and considering that KET at low doses has been shown to rescue some of the behavioral deficits of isolation rearing this study aimed to assess the effects of isolation stress on pre- and post-synaptic hippocampal functions in male and female rats reared in SIS, as well as determine whether some of the physiological deficits can be rescued with a single injection of sub-anesthetic doses of KET. To do this, Sprague-Dawley rats were raised from weaning in either social isolation or with same-sex cage mate for 5 to 7 weeks. Male and female rats in either diestrus of proestrus received a single injection of KET (0, 2.5, or 5.0 mg/kg) three hours prior to termination and collection of acute hippocampal slices for ex vivo electrophysiological field potential recordings. Long-term potentiation (LTP) and paired pulse facilitation (PPF) outputs were assessed in a canonical CA3-CA1 dorsal hippocampal circuit. Our data show that SIS inhibits hippocampal LTP without affecting PPF in male rats, an effect that was rescued by KET. In female rats, isolation stress did not alter LTP, but did reduce PPF - especially when females were tested in diestrus-, an effect that was rescued by KET at the highest dose. Our data thus suggest sex differences in the contribution of pre-and postsynaptic hippocampal compartments in response to stress and KET.

Project description:Intergenerational plasticity or parental effects-when parental environments alter the phenotype of future generations-can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex-of both the parent and the offspring-plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.

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Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish.

Publications

Sex-specific effects of psychoactive pollution on behavioral individuality and plasticity in fish.

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