The behavioral immune system in grey mouse lemurs: Causes of individual variation in behavioral defenses and consequences for socio-ecological traits
Evolution, Anthropology
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Final Report Abstract
Behavioral immunity refers to a set of avoidance strategies that limit contact with pathogens before infection occurs. This system represents a first line of defense, allowing individuals to reduce infection risk through flexible behaviors such as avoiding contaminated food, infected conspecifics, or risky environments. However, these behaviors incur costs. Avoidance behaviors might, for instance, reduce foraging intake, sheltering opportunities or mate availability, explaining the existence of different ‘hygienic types’. Therefore, their expression likely results from trade-offs between benefits in parasite avoidance and costs to other vital functions, and can vary according to individual traits (e.g., sex, age, social rank, genetic susceptibility, physiological state) and environmental context (e.g., food availability, seasonality). However and despite its importance, and relative to the volume of research on the determinants influencing physiological immuno-competence, little empirical work has aimed at measuring individual investment in behavioral immunity so far, and the determinants affecting individual variation remain poorly explored. In several species, including humans, females tend to show stronger behavioral defenses than males, likely reflecting different evolutionary pressures: increased investment in immunity in females to support longevity, and in reproduction for males. According to the ‘compensatory prophylaxis hypothesis’, behavioral immunity may be upregulated when physiological immunity is compromised, such as during early pregnancy or seasonal torpor. While there is some indirect support for this idea, empirical evidence remains limited, and little is known about how behavioral immunity and physiological immunity interact in wild populations. According to the ‘density-dependent prophylaxis hypothesis’, the effect of group size on infection risk may generate a selective pressure that select for increased immunity in gregarious animals. While this hypothesis has received support from several empirical studies, many exceptions have been reported. This could be partly explained by a higher investment of social species in behavioral defenses, which are usually ignored in studies testing this hypothesis. As behavioral defenses are suspected to incur a lower energetic cost than physiological defenses, it has even been proposed that animals living in groups could favor investment in the behavioral rather than physiological component of immune defense. However, this hypothesis remains untested in vertebrates as no study has investigated whether group-living animals invest more in behavioral defenses than their solitary counterparts. To address this gap, I investigated individual variation in behavioral defenses against parasites in the grey mouse lemur (Microcebus murinus), a small Malagasy primate. This species, exhiting a facultative sociality, provides a valuable model for studying behavioral immunity in both wild and captive settings, and allows testing key hypotheses at the interface of behavioral ecology, immunology, and disease dynamics.
Publications
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Hygienic personalities in wild grey mouse lemurs vary adaptively with sex. Proceedings of the Royal Society B: Biological Sciences, 286, 20190863.
Poirotte, Clémence & Kappeler, Peter M.
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Same father, same face: Deep learning reveals selection for signaling kinship in a wild primate. Science Advances, 6(22).
Charpentier, M. J. E.; Harté, M.; Poirotte, C.; de Bellefon, J. Meric; Laubi, B.; Kappeler, P. M. & Renoult, J. P.
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Unconditional care from close maternal kin in the face of parasites. Biology Letters, 16(2).
Poirotte, Clémence & Charpentier, Marie J. E.
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Environmental and individual determinants of fecal avoidance in semi‐free ranging woolly monkeys (Lagothrix lagotricha poeppigii). American Journal of Physical Anthropology, 176(4), 614-624.
Philippon, Justine; Serrano‐Martínez, Enrique & Poirotte, Clémence
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Mandrill mothers associate with infants who look like their own offspring using phenotype matching. eLife, 11.
Charpentier, Marie JE; Poirotte, Clémence; Roura-Torres, Berta; Amblard-Rambert, Paul; Willaume, Eric; Kappeler, Peter M.; Rousset, François & Renoult, Julien P.
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Fecal avoidance and gastrointestinal parasitism in semi-free ranging woolly monkeys (Lagothrix lagotricha poeppigii). Behavioral Ecology and Sociobiology, 77(4).
Philippon, Justine; Serrano-Martínez, Enrique & Poirotte, Clémence
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Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills. Proceedings of the Royal Society B: Biological Sciences, 290.
Poirotte, Clémence & Charpentier, Marie J. E.
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Who to sleep with? Daytime sleeping associations in nocturnal gray mouse lemurs. Behavioral Ecology and Sociobiology, 79(6).
Engelhardt, Sacha C.; Socias-Martínez, Lluís; Poirotte, Clémence; Bodson, Pauline; Sinaotse, Gregoire; Ampataka, Rémi; Peckre, Louise; Lahmann, Henning; Mosna, Marta; Ratsoavina, Fanomezana Mihaja; Fichtel, Claudia & Kappeler, Peter M.
