What Happens after Inbreeding Avoidance? Inbreeding by Rejected Relatives and the Inclusive Fitness Benefit of Inbreeding Avoidance

April What Happens after Inbreeding Avoidance? Inbreeding by Rejected Relatives and the Inclusive Fitness Benefit of Inbreeding Avoidance A. Bradley Duthie 0 1 2 Jane M. Reid 0 1 2 0 Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen , Aberdeen , United Kingdom 1 Funding: This work was funded by a European Research Council Grant (http://erc.europa.eu/erc- funded-projects) and a Royal Society University Research Fellowship (www.royalsociety.org) to Jane M. Reid. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 2 Academic Editor: Theresa M. Jones, University of Melbourne , AUSTRALIA Avoiding inbreeding, and therefore avoiding inbreeding depression in offspring fitness, is widely assumed to be adaptive in systems with biparental reproduction. However, inbreeding can also confer an inclusive fitness benefit stemming from increased relatedness between parents and inbred offspring. Whether or not inbreeding or avoiding inbreeding is adaptive therefore depends on a balance between inbreeding depression and increased parent-offspring relatedness. Existing models of biparental inbreeding predict threshold values of inbreeding depression above which males and females should avoid inbreeding, and predict sexual conflict over inbreeding because these thresholds diverge. However, these models implicitly assume that if a focal individual avoids inbreeding, then both it and its rejected relative will subsequently outbreed. We show that relaxing this assumption of reciprocal outbreeding, and the assumption that focal individuals are themselves outbred, can substantially alter the predicted thresholds for inbreeding avoidance for focal males. Specifically, the magnitude of inbreeding depression below which inbreeding increases a focal male0s inclusive fitness increases with increasing depression in the offspring of a focal female and her alternative mate, and it decreases with increasing relatedness between a focal male and a focal female0s alternative mate, thereby altering the predicted zone of sexual conflict. Furthermore, a focal male0s inclusive fitness gain from avoiding inbreeding is reduced by indirect opportunity costs if his rejected relative breeds with another relative of his. By demonstrating that variation in relatedness and inbreeding can affect intra- and intersexual conflict over inbreeding, our models lead to novel predictions for family dynamics. Specifically, parent-offspring conflict over inbreeding might depend on the alternative mates of rejected relatives, and male-male competition over inbreeding might lead to mixed inbreeding strategies. Making testable quantitative predictions regarding inbreeding strategies occurring in nature will therefore require new models that explicitly capture variation in relatedness and inbreeding among interacting population members. - Competing Interests: The authors have declared that no competing interests exist. Inbreeding, defined as mating between related individuals, is a pervasive force in evolutionary ecology that is postulated to drive the evolution of mating systems [13] and dispersal [4, 5], and to influence population dynamics [6, 7] and the expression and persistence of mutation load [8, 9]. Understanding these phenomena therefore requires a thorough understanding of the evolution and occurrence of inbreeding itself. Reproducing individuals might exhibit strategies of inbreeding preference or avoidance defined as mating with more or less closely related individuals than expected given random mating, or exhibit inbreeding tolerance defined as random mating with respect to relatedness [10]. In general, the evolution of any such inbreeding strategy is expected to depend on the balance between increased inheritance of identical-by-descent alleles by inbred offspring versus any decrease in survival or reproductive fitness of those inbred offspring due to inbreeding depression. This balance is well understood in the context of the evolution of self-fertilisation versus outcrossing [1116]. Specifically, in an outcrossing population, a mutant allele causing self-fertilisation (the most extreme degree of inbreeding) is 50% more likely to be inherited identicalby-descent by the selfing individual0s offspring than a homologous wild type allele underlying outcrossing, but resulting inbred offspring will commonly show inbreeding depression [2, 12, 13, 17]. The net inclusive fitness benefit of self-fertilisation, and hence the frequency of the underlying mutant allele, will therefore depend on the balance between increased offspring inheritance of identical-by-descent alleles versus reduced offspring survival or reproductive fitness [12, 13, 1518]. The net inclusive fitness benefit of biparental inbreeding (i.e., inbreeding between two nonself individuals) depends on this same balance. Inbreeding depression is widespread and can substantially reduce offspring fitness in populations with biparental fertilisation [7, 19, 20]. Consequently, inbreeding depression is widely presumed to drive the evolution of inbreeding avoidance in such populations [12, 2123]. But the inclusive fitness increment of biparental inbreeding relative to outbreedingwhich stems from the higher probability that identical-bydescent alleles will be inherited by inbred offspringhas been less widely factored into verbal or quantitative models regarding the evolution of biparental inbreeding versus inbreeding avoidance [10]. Models examining the evolution of self-fertilisation cannot be directly extrapolated to predict the evolution of biparental inbreeding strategy because they do not account for sex-specific inclusive fitness benefits or differing reproductive strategies between males and females with potentially conflicting evolutionary interests [10]. Instead, Parker [24, 25] provided a basic conceptual model that specifically emphasised the inclusive fitness benefit of biparental inbreeding stemming from increased probability of identity-by-descent, and this model was subsequently extended by Waser et al. [26], Kokko and Ots [27], and Puurtinen [28]. These models emphasise that inbreeding preference or tolerance might be adaptive even when inbreeding depression occurs. They also predict evolutionary sexual conflict over inbreeding, meaning that selection on inbreeding preference, tolerance, or avoidance might differ between males and females [24, 25]. This sexual conflict arises because reproductive investment in inbred offspring differentially affects the mean inclusive fitness of each sex (assuming different sex roles). If an individual of the sex whose reproduction is limited by resource availability inbreeds, resources will be invested in less fit inbred offspring instead of fitter outbred offspring. In contrast, an individual of the sex whose reproduction is limited by mate availability might be able to inbreed with (...truncated)