Inbreeding in the wild: a cost-benefit analysis

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It is well known that mating between related individuals, known as inbreeding, gives rise to unhealthy offspring, a phenomenon termed inbreeding depression, and many human cultures have taboos against marriages between close relatives. Similarly, many species appear to have evolved mechanisms to avoid inbreeding - for example the famous 'pin' and 'thrum' flowers of primroses that ensure pollination by a different plant. However, at the opposite extreme, many plants and some animals, for example some species of snail, are hermaphrodite (having male and female parts in the same individual) and regularly self-fertilise, so they inbreed intensively. This demonstrates that, as with many things in biology, inbreeding has evolutionary benefits as well as costs. One of the main benefits arises because inbred offspring share more of their genome with their parents than outbred offspring: inbreeding therefore increases the representation of an individual's genes in the next generation, its so-called 'inclusive fitness'. There is well-developed theory about this trade-off between the costs and benefits of inbreeding, which indicates that inbreeding should not necessarily be avoided as much as we might assume. In line with this, several recent studies, including our own work on red deer, show a lack of inbreeding avoidance in populations that show inbreeding depression. However, to date empirical studies of inbreeding have paid little attention to the potential benefits of inbreeding, focussing instead on its costs. Furthermore, even the costs of inbreeding are likely to have been underestimated, due to relatively inaccurate methods for assessing how inbred an individual is. Using our study population of red deer on the Isle of Rum, NW Scotland, we will conduct one of the first comprehensive investigations of the costs and benefits of inbreeding in a natural population. In red deer, successful males mate with several females during a short annual mating season, and females then provide all of the parental care. Theory suggests that in a polygynous system such as this, in which a female produces only one calf a year, females should be less tolerant of inbreeding because mating with a relative forfeits an outbred mating - in contrast, for males, there is no cost of forfeited matings. Current estimates indicate a higher-than-expected frequency of inbred matings (42%) in our study population, given that the resulting inbred offspring have lower fitness. The aim of the current project is to investigate this apparently-paradoxical observation in light of the theoretical models, and in doing so to provide novel insights into the factors shaping mating behaviour, dispersal patterns and inbreeding depression in a wild mammal. The proposed research will exploit a combination of new genetic tools, long-term monitoring records and new behavioural data. We will have access to a genome-wide DNA profile for each individual which will dramatically improve our ability to detect inbreeding and hence inbreeding depression. The red deer rut comprises a complex mating system with the potential for numerous factors, many of which we do not yet fully understand, to affect mating decisions. We will therefore also conduct detailed observations of behaviour during the mating season to determine levels of inbreeding avoidance or tolerance by each sex, with particular attention to the role of male dispersal and local movement by both sexes in the rut. Ultimately, we will be able to measure the costs (in terms of inbreeding depression) and benefits (in terms of increased inclusive fitness) of inbreeding in the red deer study population. This will allow us to determine how tolerant each sex should be of inbreeding, and hence to test, for the first time in any population, whether observed levels of inbreeding reflect optimal choice of mates.