Inbreeding and its avoidance in a wild bird population

Inbreeding occurs when relatives mate and have offspring. Inbreeding depression is hypothesized to have influenced the evolution of mating systems and behavioural mechanisms of inbreeding avoidance in the animal kingdom. Inbreeding in the wild is difficult to measure, as in order to build a pedigree allowing us to identify matings between relatives, the identity of as many as possible members of a population needs to be known. For a long time, the main source of knowledge about inbreeding depression was based on laboratory and agricultural studies, which did not reflect the array of environmental pressures wild populations have to cope with. In consequence, the deleterious consequences of inbreeding have often been underestimated. This is problematic because accurate estimates of the effect size of inbreeding depression are needed to study the strength of selection on inbreeding avoidance mechanisms, and are also of importance to conservation genetics. The aim of this thesis was to use pedigree data to infer the occurrence and effects of inbreeding using over forty years of breeding events of the great tit Parus major from Wytham Woods, Oxfordshire. The effects of inbreeding on fitness were investigated across a life-history continuum, and across environments. I found that close inbreeding (f=0.25) resulted in pronounced inbreeding depression, which acted independently on hatching success, fledging success, and recruitment success, and reduced the number of fledged grand-offspring by 55%. My results therefore suggest that estimates of fitness costs of inbreeding must focus on the entire life cycle. I also show that the variation in the strength of inbreeding depression varies across environments, particularly so the more the environmental variable considered is linked to fitness. These results emphasise the need of using relevant environmental contrasts when investigating inbreeding by environment interactions. I further asked whether individuals involved in matings with relatives differed relative to individuals mating with unrelated partners. I did not find any evidence for clear predictors of inbreeding, and I show that inbreeding depression in our population is entirely independent of any tendency for low quality parental genotypes, or phenotypes, to inbreed. Neither did I find any evidence for active inbreeding avoidance: great tits did not mate less often with kin than expected based on several scenarios of random mating, nor did I find increased rates of extra-pair paternity among birds breeding with relatives. In fact, I observed quite the contrary, as birds mating with kin exhibited a higher than average rate of close inbreeding relative to all scenarios of random mating investigated, showed lower rates of extra-pair paternity and divorce than birds mated to unrelated partners. I hypothesise that cases of occasional inbreeding in this population may result from mis-imprinting or a related process whereby some birds develop particularly strong bonds that are at odds with all predictions of avoiding inbreeding. Finally, I asked to what extent natal dispersal, a behaviour that is often hypothesized to play an important role in avoiding inbreeding, indeed reduces the likelihood of inbreeding. I found that male and female individuals breeding with a relative dispersed over several-fold shorter distances than those outbreeding. This led to a 3.4 fold increase (2.3-5, 95% CI) in the likelihood of close inbreeding relative to the population average when individuals dispersed less than 200m. This thesis demonstrates that inbreeding has deleterious effects on a wild population of birds, occurring throughout an individual’s life, and is of varying strength across environments. My findings strongly support the theory that natal dispersal should be considered as a mechanism of prime importance for inbreeding avoidance.

Keywords: great tit
divorce
inbreeding avoidance
extra-pair paternity
random mating
inbreeding
Parus major
Wytham
genotype environment interactions
inbreeding depression
dispersal
Advisor: Sheldon, B