Dispersal as a means of inbreeding avoidance in a wild bird population

Marta Szulkin () 0 Ben C. Sheldon 0 0 Edward Grey Institute, Department of Zoology, University of Oxford , Oxford OX1 3PS , UK The long-term study of animal populations facilitates detailed analysis of processes otherwise difficult to measure, and whose significance may appear only when a large sample size from many years is available for analysis. For example, inbreeding is a rare event in most natural populations, and therefore many years of data are needed to estimate its effect on fitness. A key behaviour hypothesized to play an important role in avoiding inbreeding is natal dispersal. However, the functional significance of natal dispersal with respect to inbreeding has been much debated but subject to very few empirical tests. We analysed 44 years of data from a wild great tit Parus major population involving over 5000 natal dispersal events within Wytham Woods, UK. Individuals breeding with a relative dispersed over several-fold shorter distances than those outbreeding; within the class of inbreeding birds, increased inbreeding was associated with reduced dispersal distance, for both males and females. This led to a 3.4-fold increase (2.3-5, 95% CI) in the likelihood of close ( fZ0.25) inbreeding relative to the population average when individuals dispersed less than 200 m. In the light of our results, and published evidence showing little support for active inbreeding avoidance in vertebrates, we suggest that dispersal should be considered as a mechanism of prime importance for inbreeding avoidance in wild populations. 1. INTRODUCTION Natal dispersal, defined as the distance moved by an individual from its birth place to the site of its first reproduction (Howard 1960; Greenwood 1980; Clobert et al. 2001), is a key life-history event with relevance for many aspects of evolutionary biology, ecology and conservation biology: it alters gene flow; changes allele frequencies within and among populations (Clobert et al. 2001) and influences the distribution and abundance of organisms ( Johnson & Gaines 1990). Three factors are most often proposed to be important contributors towards the evolution of dispersal (Gandon & Michalakis 2001). Dispersal may have evolved in order to reduce competition between relatives (Hamilton & May 1977), owing to the temporal variability of the environment (Olivieri et al. 1995; Gandon & Michalakis 1999) or it may function as a means of inbreeding avoidance. The consequence of inbreeding, defined as the mating of individuals sharing ancestors ( Wright 1922), is increased genome-wide homozygosity. This, in turn, causes inbreeding depression, which is mediated either through overdominance (where heterozygous individuals have superior fitness relative to homozygous equivalents) or most often due to the expression of deleterious recessive alleles (Lynch & Walsh 1998; Charlesworth & Charlesworth 1999; Keller & Waller 2002). Thus, in the absence of other mechanisms of inbreeding avoidance, the act of dispersing from its natal site may substantially reduce the likelihood of choosing a related individual for mate. Many studies have investigated the relationship between inbreeding and dispersal from a theoretical standpoint (Bulmer 1973; Bengtsson 1978; Waser et al. 1986; Motro 1991; Gandon 1999; Perrin & Mazalov 1999, 2000; Roze & Rousset 2005; Guillaume & Perrin 2006). The outcome of these theoretical studies varies greatly depending on their initial assumptions. Ultimately, this leads to a trade-off between simple models with reduced realism, or complex models where estimating the relative importance of each parameter and the size of interactions between them becomes increasingly difficult (Gandon & Michalakis 2001). Using a game-theoretical approach, Perrin & Mazalov (1999) emphasized that inbreeding by itself is unlikely to account for the evolution of dispersal on its own. Undoubtedly, there is much more to dispersal than just inbreeding avoidance; the question is not whether inbreeding affects dispersal or not, but in what way and by how much (Perrin & Goudet 2001). It is clear that there is a need for empirical studies that explore the interplay between inbreeding and dispersal; such tests should ideally be carried out in a natural setting, where dispersal is under natural selection. The number of theoretical studies on inbreeding and dispersal contrasts markedly with the very few empirical studies where the costs of inbreeding, and the importance of dispersal as a mean of inbreeding avoidance, have been estimated (Greenwood et al. 1978; Schiegg et al. 2006). This paucity of empirical studies is probably partly due to the fact that in order to test the relative importance of inbreeding on the evolution of dispersal, very large numbers of dispersal events, together with a continuous monitoring of a population over a long time scale, are required. Greenwood et al. (1978) explored the relationship between inbreeding depression and natal dispersal using 11 years of data from the long-term study of great tits in Wytham Woods. However, their study did not formally test relationships between inbreeding and dispersal, and only a limited number of inbreeding pairs were identified for which natal dispersal distances could be investigated. The aim of the present study was to use a much more extensive dataset for the same population, involving over 5000 dispersal events recorded over 44 years, to test the relationship between dispersal and inbreeding at different levels. In a previous study, we showed that close inbreeding in this population reduces fitness by 55%, calculated in terms of the number of fledged grand-offspring relative to an outbred pair (Szulkin et al. 2007). Here, we demonstrate a strong effect of limited natal dispersal on the likelihood of inbreeding, and suggest that dispersal should be considered a fundamental mechanism of inbreeding avoidance in many vertebrate species. 2. MATERIAL AND METHODS (a) Study population The great tit Parus major is a small hole nesting passerine bird that has been studied at Wytham Woods (Oxfordshire, UK, 18200 W 518460 N) since 1947 (Perrins 1979). The population breeds almost exclusively in over 1000 artificial nestboxes, scattered at variable densities across ca 380 ha of semi-natural deciduous woodland. The number and location of nest-boxes throughout the site, as well as the breeding protocol, have remained fairly constant since 1964; the exact coordinates of all nest-boxes were digitally mapped in 2005 ( Wilkin et al. 2006). Great tit breeding events are identified by performing regular checks of all nest-boxes in the study area throughout the breeding season. Nestlings are ringed 15 days after hatching, and parents caught and identified while feeding young at the nest. Immigration rates into the population are relatively high, as on average 40% of males and 47% of females breeding in any year within Wytham are born outside the forest (McCleery et al. 2004); immigrants are assumed to be (...truncated)