Inbreeding in the wild: a cost-benefit analysis

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.

Who will benefit?

We see three major groupings of beneficiaries from the proposed research.
1) Conservation biologists
2) Wildlife managers managing abundant and hunted vertebrates
3) The general public.

How will they benefit?

1) Conservation biologists: as outlined in the proposal, the severity of inbreeding depression and the strength of interactions between inbreeding depression and environmental heterogeneity may have been substantially underestimated in natural populations. Similarly, the concept that organisms may naturally tolerate inbreeding to maximise inclusive fitness is not widely considered. Our research will provide novel information on the strength of inbreeding depression and the degree to which it is tolerated in a natural population that will be of great importance to those in the conservation community that are faced with complex management problems, often with relatively little information on their own population. We aim to provide hard facts and figures on these phenomena for a representative large mammal, and use this information to improve the understanding of inbreeding and inbreeding depression in the conservation community.

2) Wildlife managers: the management of hunted and/or over-abundant species involves many actions based on understanding the basic biology of the species in question. For example, many vertebrates are managed on the basis that males disperse to avoid inbreeding and that inbreeding is avoided. Depending on our findings, our study will be able to refine such views, for example by demonstrating that male dispersal for the purposes of feeding is not the same as breeding dispersal.

3) The general public: The general public has a great interest in understanding the complex behaviours we see in natural populations. This research will provide a unique insight into the causes and consequences of the behaviour of one of the UK's most charismatic large mammals during one of the most spectacular episodes of its life cycle, the annual rut. The public are also generally interested in genetics and especially inbreeding, and our research should help understanding of the complexities of inbreeding in nature.

How will we engage with these groups?

1) Conservation biologists: Our impacts will be relevant to those measuring inbreeding's consequences in threatened populations, those developing conservation policy and those educating on the principles of population conservation, and we aim to influence this field by presenting the work in the appropriate journals and at conservation science conferences.

2) Wildlife managers: At one level, we will again aim to have impact at the scientific level by publishing in journals such as the Journal of Wildlife Management. At a more practical and local level, we will attend events run by SNH and the deer management community which are designed to receive views from stakeholders, to deliver continuing professional development to deer managers and to bring scientists and stakeholders together. We will attend selected events early in the project to engage with stakeholders and get more detailed input on their angles of interest in our project, and then again at the end of the project to report back on our findings and their operational implications.

3) The general public. We intend to engage with and educate the general public by a wide range of methods including: on the Isle of Rum, by enhancing our facilities, documentation and presentations for visitors and continuing to assist TV crews filming in the study area - in particular we will try to get results from this study into TV story lines. Off-island we will continue with museum and science festival exhibits, press releases to attract media attention to our research and the project website and Twitter feed.

For a more detailed description please see the 'Pathways to Impact' document.