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

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.