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Open Access Highly Accessed Research article

Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate

Marylène Boulet14, Marie JE Charpentier12 and Christine M Drea13*

  • * Corresponding author: Christine M Drea cdrea@duke.edu

  • † Equal contributors

Author Affiliations

1 Department of Evolutionary Anthropology, 108 BioSci BLDG, Box 90383, Duke University, Durham, North Carolina, 27708, USA

2 CEFE-CNRS, 1919 Route de Mende, 34293 Montpellier Cedex 5, France

3 Department of Biology, 108 BioSci BLDG, Box 90383, Duke University, Durham, North Carolina, 27708, USA

4 Department of Biology, Bishop's University, 2600 College Street, Sherbrooke, Québec, J1M 1Z7, Canada

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BMC Evolutionary Biology 2009, 9:281  doi:10.1186/1471-2148-9-281

Published: 3 December 2009

Abstract

Background

Like other vertebrates, primates recognize their relatives, primarily to minimize inbreeding, but also to facilitate nepotism. Although associative, social learning is typically credited for discrimination of familiar kin, discrimination of unfamiliar kin remains unexplained. As sex-biased dispersal in long-lived species cannot consistently prevent encounters between unfamiliar kin, inbreeding remains a threat and mechanisms to avoid it beg explanation. Using a molecular approach that combined analyses of biochemical and microsatellite markers in 17 female and 19 male ring-tailed lemurs (Lemur catta), we describe odor-gene covariance to establish the feasibility of olfactory-mediated kin recognition.

Results

Despite derivation from different genital glands, labial and scrotal secretions shared about 170 of their respective 338 and 203 semiochemicals. In addition, these semiochemicals encoded information about genetic relatedness within and between the sexes. Although the sexes showed opposite seasonal patterns in signal complexity, the odor profiles of related individuals (whether same-sex or mixed-sex dyads) converged most strongly in the competitive breeding season. Thus, a strong, mutual olfactory signal of genetic relatedness appeared specifically when such information would be crucial for preventing inbreeding. That weaker signals of genetic relatedness might exist year round could provide a mechanism to explain nepotism between unfamiliar kin.

Conclusion

We suggest that signal convergence between the sexes may reflect strong selective pressures on kin recognition, whereas signal convergence within the sexes may arise as its by-product or function independently to prevent competition between unfamiliar relatives. The link between an individual's genome and its olfactory signals could be mediated by biosynthetic pathways producing polymorphic semiochemicals or by carrier proteins modifying the individual bouquet of olfactory cues. In conclusion, we unveil a possible olfactory mechanism of kin recognition that has specific relevance to understanding inbreeding avoidance and nepotistic behavior observed in free-ranging primates, and broader relevance to understanding the mechanisms of vertebrate olfactory communication.