Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens KEITH A. TARVIN * , MICHAEL S. WEBSTER †, ELAINA M. TUTTLE ‡ & STEPHEN PRUETT-JONES § *Department of Biology, Oberlin College ySchool of Biological Sciences and Center for Reproductive Biology, Washington State University, Pullman zDepartment of Life Sciences, Indiana State University, Terre Haute xDepartment of Ecology and Evolution, University of Chicago (Received 7 April 2004; initial acceptance 8 June 2004; final acceptance 27 January 2005; MS. number: A9855R) Why females mate with multiple males, particularly in socially monogamous species, is one of the central unanswered questions in sexual selection and behavioural ecology. Recent theory suggests that socially monogamous females may improve the genetic quality of their offspring by mating with extrapair males with whom they are more genetically dissimilar (relative to their social mates), because decreased genetic similarity between mates may lead to decreased inbreeding depression of offspring and other benefits. We found that levels of extrapair paternity in splendid fairy-wren, Malurus splendens, broods were predicted by genetic similarity between social mates. Females whose entire broods were sired by extrapair males were more genetically similar to their social mates than they were to their extrapair mates, but females were no less similar to their extrapair mates than they were to the average male from the population. Within-pair young (WPY) from mixed-paternity broods showed higher levels of inbreeding and lower heterozygosity than did their extrapair nestmates or WPY from broods without extrapair paternity. Several processes could account for these patterns, including female choice of genetically dissimilar mates, differential sperm investment by males or differential survival of embryos as a function of genetic dissimilarity between mates, or postcopulatory processes such as sperm competition, cryptic female choice, or interactions between sperm and ova. Regardless of the mechanism, our results suggest that female splendid fairy-wrens may indirectly benefit from extrapair mating because it leads to lower levels of inbreeding and increased heterozygosity in their offspring. Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Although males can increase their fecundity by mating with multiple partners, the same is generally not true for females, and why females mate with multiple males remains one of the central unanswered questions in behavioural ecology and sexual selection (Zeh & Zeh 1996; Petrie & Kempenaers 1998; Jennions & Petrie 2000; Tregenza & Wedell 2000; Griffith et al. 2002; Griffith & Montgomerie 2003). This is particularly true for species in which females form social pair bonds with males but also copulate with males outside of the social pair (‘extrapair males’). For example, the vast majority of birds are socially monogamous, and yet in approximately 75% of such species, females copulate with extrapair males as well as with their social partners (Griffith et al. 2002). This lack of concordance between genetic and social mating systems has led to considerable research focusing on birds as a model system for understanding the function of extrapair copulations and multiple mating by females in general. Many studies have tested ‘good genes’ and Fisherian hypotheses for extrapair mating, which predict that females copulate with extrapair males bearing phenotypic traits indicative of good health or attractiveness. Although many of these studies have found support for good genes models, many others have failed to demonstrate a clear relationship between male phenotypic traits and extrapair mating success (reviewed in Griffith et al. 2002), suggest- ing that extrapair mating may sometimes occur for reasons other than those proposed by traditional sexual selection models. An alternative to traditional explana- tions for extrapair mating is the proposal that females can improve the viability of their offspring by mating with Correspondence: K. A. Tarvin, Department of Biology, Oberlin College, Oberlin, OH 44074, U.S.A. (email: keith.tarvin@oberlin.edu). 945 0003–3472/05/$30.00/0 Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. ANIMAL BEHAVIOUR, 2005, 70, 945–955 doi:10.1016/j.anbehav.2005.01.012