The role of immune-mediated female sperm selection in temporal dynamics of fertilisation bias

父权在雄性间的分配方式对种群的生态和进化具有重要影响，调节着种群的有效规模和现存遗传变异的数量。尽管对繁殖成功的强烈选择，父权仍然是高度可变的，理解这种变化的机制是生物学的一个基本挑战。越来越多的证据表明，父权变异的一个重要来源源于受精后发生的过程。在大多数生物中，多个雄性的射精经常竞争使一组卵子受精，而雌性可以通过对不同雄性精子的偏见反应，极大地影响这种竞争的结果。为了提高后代的成功率，雌性会偏向于选择遗传质量较高的雄性。由于个体的遗传多样性（杂合性）促进了生存，一个越来越流行的假说是，雌性优先利用与雌性基因不同的雄性精子来促进后代的杂合性。然而，这一假设的证据是模糊的，与理论相反，女性可能经常倾向于受精，而不是遗传相似的男性。最近来自不同物种的证据，包括我们自己对红色丛林鸮的研究表明，这种违反直觉的反应可能是由主要组织相容性复合体（MHC）的遗传相似性调节的。MHC是一种基因复合体，在免疫反应中起着重要作用，使生物体能够从非自我中识别自我，并对不被识别为自我的细胞做出反应。虽然这种免疫反应使生物体能够对抗病原体和寄生虫，但它也可能导致对不同男性精子的不同反应。也就是说，我们期望女性免疫系统能够容忍与女性具有相同MHC基因的男性的精子，而歧视具有不同MHC基因的男性的精子。由于这是典型的相似免疫反应，我们也预计雌性对与雌性具有一定MHC相似性的精子的反应会随着雌性与同一类型精子的连续授精而改变。这似乎是合理的，通过持续接触，女性免疫系统“学会”识别mhc相似的精子类型，从而减少了父亲的偏见。这一新颖的假设是建立在完善的免疫机制基础上的，它代表了一种生物学上合理的近似解释，与研究的新趋势一致，表明受精可能偏向于基因相似的伴侣。因此，阐明mhc介导的免疫反应对女性精子选择的影响将有助于揭示自然种群中父权变异的机制。这项拟议研究的目的是通过实验来验证受精是由mhc介导的女性生殖道对不同男性射精的免疫反应所影响的假设的不同关键预测。我们将在一个特征良好的红色丛林鸟种群中测试这些预测。红丛林鸡是家鸡的野生祖先，是研究mhc介导的雌性精子选择的理想系统。首先，女性通常会从多个男性那里获得射精，并且以不同的方式偏爱受精，包括偏爱mhc相似的精子。其次，家禽人工授精和精子分析技术使我们能够在受控条件下无创地研究授精后过程。第三，鸡的MHC非常简单，特征非常明显。最后，我们对该物种中调节父权偏斜的机制有了深入的了解，包括MHC相似性的作用。

The way paternity is distributed across males has considerable impact on the ecology and evolution of a population, regulating the effective population size and the amount of standing genetic variance. Despite intense selection on reproductive success paternity remains highy variable, and understanding the mechanisms underpinning this variation is a fundamental challenge in Biology. Increasing evidence indicates that an important source of variation in paternity originates from processes occurring after insemination. In most organisms the ejaculates of multiple males often compete to fertilise a set of eggs, and females can drastically influence the outcome of this competition through biased responses to the sperm of different males. Females are expected to bias fertilisation in favour of males of higher genetic quality in order to increase the success of their offspring. Because the genetic diversity (heterozyosity) of an individual promotes survival, a increasingly topical hypothesis is that females preferentially utilise the sperm of males that are genetically different from the female to promote offspring heterozygosity. However, evidence for this hypothesis is ambiguous and -contrary to theory- females may often bias fertilisation in favour of genetically similar rather than dissimilar males. Recent evidence from different species including our own work in the red junglefowl indicates that this counterintuitive response may be regulated by genetic similarity at the Major Histocompatibility Complex (MHC). The MHC is a complex of genes that play a fundamental role in immune responses allowing the organism to recognise self from non-self and respond against cells that are not recognised as self. While this immune response enables the organism to combat pathogens and parasites it may also result in a side-effect differential response to sperm of different males. Namely, we expect the female immune system to tolerate sperm of males that share MHC genes with the female and discriminate against the sperm of males that have a different MHC profile. As it is typical of similar immune responses, we also expect female response to the sperm of a certain MHC similarity with the female to change as the female is exposed to successive inseminations with the same type of sperm. It is plausible that, through continued exposure, the female immune system 'learns' to recognise MHC-similar sperm type, thus reducing the bias in paternity. This novel hypothesis is founded on well established immunological mechanisms and represents a biologically plausible proximate explanation consistent with an emergent trend of studies indicating that fertilisation may be biased in favour of genetically similar partners. Elucidating the consequences of MHC-mediated immune responses for female sperm selection would therefore contribute to unravel the mechanisms underpinning variation in paternity in natural populations. The aim of the proposed research is to test experimentally different key predictions of the hypothesis that fertilisation is biased by MHC-mediated immunological responses of the female reproductive tract to the ejaculates of different males. We will test these predictions in a well characterised population of red junglefowl. Red junglefowl are the wild ancestor of the domestic chicken and an ideal system to study MHC-mediated female sperm selection. First, females typically obtain ejaculates from multiple males and are known to bias fertilisation in different ways, including in favour of MHC-similar sperm. Second, poultry techniques of artificial insemination and sperm assays enable us to study post-insemination processes non-invasively and under controlled conditions. Third, the MHC of the fowl is very simple and extremely well characterised. Finally, we have a deep understanding of the mechanisms that modulate paternity skews in this species, including the role of MHC similarity.