Inbreeding in the wild: a cost-benefit analysis

众所周知，相关个体之间的交配，即所谓的近亲繁殖，会产生不健康的后代，这种现象称为近亲繁殖抑郁症，许多人类文化对近亲之间的婚姻有禁忌。同样，许多物种似乎已经进化出避免近亲繁殖的机制-例如著名的报春花的“针”和“线”花，以确保由不同的植物授粉。然而，在另一个极端，许多植物和一些动物，例如一些蜗牛，是雌雄同体的（在同一个体中有雄性和雌性部分），并且定期自花受精，所以它们密集地近亲繁殖。这表明，就像生物学中的许多事情一样，近亲繁殖既有进化的好处，也有代价。近亲繁殖的主要好处之一是，与远交后代相比，近亲繁殖的后代与父母共享更多的基因组：因此，近亲繁殖增加了个体基因在下一代中的代表性，即所谓的“包容性适应性”。关于近亲繁殖的成本和收益之间的权衡，有一个成熟的理论，这表明近亲繁殖不一定像我们想象的那样应该避免。与此相一致的是，最近的几项研究，包括我们自己对红鹿的研究，表明在表现出近亲繁殖衰退的种群中缺乏避免近亲繁殖的行为。然而，到目前为止，近亲繁殖的实证研究很少关注近亲繁殖的潜在利益，而是关注其成本。此外，由于评估个体近交程度的方法相对不准确，甚至近亲繁殖的成本也可能被低估。使用我们的研究人口的红鹿的朗姆酒，苏格兰西北部的岛屿，我们将进行第一次全面调查的成本和效益的近亲繁殖的自然人口。在红鹿中，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，在这样一个一夫多妻制的系统中，雌性一年只产一只小牛，雌性对近亲繁殖的容忍度应该较低，因为与亲戚交配会丧失远系交配的机会--相反，对于雄性来说，丧失交配机会没有任何代价。目前的估计表明，在我们的研究人群中，近交交配的频率高于预期（42%），因为由此产生的近交后代具有较低的适应性。当前项目的目的是根据理论模型研究这一明显矛盾的观察结果，并在此过程中为野生哺乳动物中形成交配行为，传播模式和近亲繁殖抑郁症的因素提供新的见解。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。我们将获得每个个体的全基因组DNA图谱，这将大大提高我们检测近亲繁殖的能力，从而提高近亲繁殖抑郁症的能力。红鹿的发情期包括一个复杂的交配系统，其中有许多因素可能会影响交配决策，但我们还没有完全了解这些因素。因此，我们也将在交配季节进行详细的行为观察，以确定每种性别的近亲繁殖避免或容忍的水平，特别注意男性分散和本地运动的作用，由双方在车辙。最终，我们将能够衡量红鹿研究群体中近亲繁殖的成本（在近亲繁殖衰退方面）和收益（在增加包容性健身方面）。这将使我们能够确定每种性别对近亲繁殖的容忍程度，从而首次在任何种群中测试所观察到的近亲繁殖水平是否反映了对配偶的最佳选择。

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.