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

免疫介导的雌性精子选择在受精偏向的时间动态中的作用

• 批准号: NE/H008047/1
• 负责人: Tommaso Pizzari
• 金额: $ 71.71万
• 依托单位: University of Oxford
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2010
• 资助国家: 英国
• 起止时间: 2010 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FH008047%2F1
• 关键词: role; immune; mediated; female; sperm

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.

父子关系在雄性种群中的分布方式对种群的生态和进化有相当大的影响，调节着有效的种群规模和站立遗传变异量。尽管对生殖成功进行了激烈的选择，但父子关系仍然具有很高的变异性，理解这种变异的机制是生物学中的一个根本挑战。越来越多的证据表明，父子关系变异的一个重要来源是受精后的过程。在大多数生物体中，多个雄性的射精经常竞争着让一组卵子受精，而雌性可以通过对不同雄性的精子的偏向反应来极大地影响这种竞争的结果。为了提高后代的繁殖力，雌性会偏向遗传质量更高的雄性。因为个体的遗传多样性(杂合性)促进生存，一个越来越流行的假设是，雌性优先利用与雌性遗传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棱两可的，而且与理论相反，女性可能经常偏向于基因相似的男性受精，而不是不同的男性。最近来自不同物种的证据，包括我们在红色丛林鸡中的研究表明，这种违反直觉的反应可能受到主要组织相容性复合体(MHC)的遗传相似性的调节。MHC是一个基因的复合体，在免疫反应中发挥着基础性的作用，使有机体能够识别自我和非我，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有机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副作用差异反应。也就是说，我们希望女性免疫系统能容忍与女性具有相同MHC基因的男性的精子，并歧视具有不同MHC特征的男性的精子。由于这是一种典型的相似免疫反应，我们还预计，随着雌性暴露在与同一类型精子连续受精的环境中，雌性对与雌性具有一定MHC相似性的精子的反应也会发生变化。有可能的是，通过持续暴露，女性免疫系统“学会”识别类似MHC的精子类型，从而减少父子关系上的偏见。这一新的假说建立在成熟的免疫学机制基础上，代表了一种生物学上看似合理的近似解释，与一种新的研究趋势相一致，即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开自然群体中父子关系差异的机制。这项拟议的研究的目的是通过实验测试这一假说的不同关键预测，即受精是由MHC介导的女性生殖道对不同男性射精的免疫反应造成的。我们将在一个具有良好特征的红色丛林鸟种群中测试这些预测。红毛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，雌性通常从多个雄性获得射精，并以不同的方式偏向受精，包括支持类似MHC的精子。其次，家禽人工授精和精子检测技术使我们能够在受控条件下非侵入性地研究授精后的过程。第三，家禽的MHC非常简单，特征非常好。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。

项目成果

The measure and significance of Bateman's principles.

• DOI: 10.1098/rspb.2013.2973
• 发表时间: 2014-05-07
• 期刊: Proceedings. Biological sciences
• 作者: Collet JM;Dean RF;Worley K;Richardson DS;Pizzari T
• 通讯作者: Pizzari T

Within-group male relatedness reduces harm to females in Drosophila.

• DOI: 10.1038/nature12949
• 发表时间: 2014-01-30
• 期刊: Nature
• 影响因子: 64.8
• 作者: Carazo P;Tan CK;Allen F;Wigby S;Pizzari T
• 通讯作者: Pizzari T

Disentangling the causes of temporal variation in the opportunity for sexual selection.

• DOI: 10.1038/s41467-023-36536-7
• 发表时间: 2023-02-22
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Carleial, Romulo;Pizzari, Tommaso;Richardson, David S.;McDonald, Grant C.
• 通讯作者: McDonald, Grant C.

The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication.

• DOI: 10.1038/srep35864
• 发表时间: 2016-11-02
• 期刊: Scientific reports
• 影响因子: 4.6
• 作者: Borziak K;Álvarez-Fernández A;L Karr T;Pizzari T;Dorus S
• 通讯作者: Dorus S

Inbreeding removes sex differences in lifespan in a population of Drosophila melanogaster.

• DOI: 10.1098/rsbl.2016.0337
• 发表时间: 2016-06
• 期刊: Biology letters
• 影响因子: 3.3
• 作者: Carazo P;Green J;Sepil I;Pizzari T;Wigby S
• 通讯作者: Wigby S