Inbreeding in the wild: a cost-benefit analysis

众所周知，亲属之间的交配，即近亲繁殖，会产生不健康的后代，这种现象被称为近亲繁殖抑制，许多人类文化都禁止近亲结婚。同样，许多物种似乎进化出了避免近亲繁殖的机制--例如，著名的报春花的“针形”和“线形”花朵确保了不同植物的授粉。然而，在另一个极端，许多植物和一些动物，例如一些种类的蜗牛，是两性的(同一个体中有雄性和雌性部分)，经常自我受精，因此它们密集繁殖。这表明，就像生物学中的许多事情一样，近亲交配既有进化上的好处，也有代价。近亲繁殖的主要好处之一是，近亲繁殖的后代与父母分享的基因组比近亲繁殖的后代更多：因此，近亲繁殖增加了一个人的基因在下一代的表现，也就是所谓的“包容性适合度”。关于近亲交配的成本和收益之间的权衡，有成熟的理论，这表明近亲交配不一定应该像我们想象的那样被避免。与此相一致的是，最近的几项研究，包括我们自己对马鹿的研究，表明在显示近亲繁殖衰退的种群中缺乏近亲繁殖避免。然而，到目前为止，近亲交配的经验研究很少关注近亲交配的潜在好处，而是专注于其成本。此外，由于评估个体近亲繁殖程度的方法相对不准确，即使是近亲繁殖的成本也可能被低估。利用我们在苏格兰西北部朗姆岛上研究的马鹿种群，我们将对自然种群近亲繁殖的成本和收益进行第一次全面的调查。在马鹿中，成功的雄性在每年短暂的交配季节与几只雌性交配，然后雌性提供所有的父母照顾。理论表明，在这样的一夫多妻制系统中，一只雌性一年只生一头小牛，雌性应该对近亲交配的容忍度较低，因为与亲戚交配会丧失近亲交配--相比之下，对于雄性来说，没有失去交配的代价。目前的估计表明，在我们的研究人群中，近亲交配的频率高于预期(42%)，因为由此产生的近亲交配后代的适合度较低。当前项目的目的是根据理论模型调查这一表面上自相矛盾的观察结果，并在此过程中为野生哺乳动物的交配行为、扩散模式和近亲繁殖衰退的影响因素提供新的见解。这项拟议的研究将利用新的遗传工具、长期监测记录和新的行为数据的组合。我们将获得每个个体的全基因组DNA图谱，这将极大地提高我们检测近亲繁殖和近亲繁殖衰退的能力。马鹿发情包括一个复杂的交配系统，可能会有许多因素影响交配决定，其中许多因素我们还没有完全了解。因此，我们还将对交配季节的行为进行详细的观察，以确定每个性别避免或容忍近亲交配的程度，并特别注意雄性扩散和两性在发情过程中的局部迁徙所起的作用。最终，我们将能够在马鹿研究种群中衡量近亲繁殖的成本(根据近亲繁殖的抑制)和收益(根据增加的包容性适合度)。这将使我们能够确定每个性别应该对近亲繁殖的容忍程度，从而在任何种群中第一次测试观察到的近亲繁殖水平是否反映了最佳的配偶选择。

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.