Data from: Positive selection of deleterious alleles through interaction with a sex-ratio suppressor gene in African buffalo: a plausible new mechanism for a high frequency anomaly

Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints. Here we present a possible new mechanism that explains the attainment of high frequencies of deleterious alleles in the African buffalo (Syncerus caffer) population of Kruger National Park, through positive selection of these alleles that is ultimately driven by a sex-ratio suppressor. We have previously shown that one in four Kruger buffalo has a Y-chromosome profile that, despite being associated with low body condition, appears to impart a relative reproductive advantage, and which is stably maintained through a sex-ratio suppressor. Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion. We hypothesize that this body-condition-associated reproductive advantage increases the fitness of alleles that negatively affect male body condition, causing genome-wide positive selection of these alleles. To investigate this we genotyped 459 buffalo using 17 autosomal microsatellites. By correlating heterozygosity with body condition (heterozygosity-fitness correlations), we found that most microsatellites were associated with one of two gene types: one with elevated frequencies of deleterious alleles that have a negative effect on body condition, irrespective of sex; the other with elevated frequencies of sexually antagonistic alleles that are negative for male body condition but positive for female body condition. Positive selection and a direct association with a Y-chromosomal sex-ratio suppressor are indicated, respectively, by allele clines and by relatively high numbers of homozygous deleterious alleles among sex-ratio suppressor carriers. This study, which employs novel statistical techniques to analyse heterozygosity-fitness correlations, is the first to demonstrate the abundance of sexually-antagonistic genes in a natural mammal population. It also has important implications for our understanding not only of the evolutionary and ecological dynamics of sex-ratio distorters and suppressors, but also of the functioning of deleterious and sexually-antagonistic alleles, and their impact on population viability.

尽管有害等位基因（deleterious alleles）通常较为罕见，但它们可通过遗传漂变（genetic drift）、遗传搭车效应（hitchhiking）或选择约束（selective constraints）的减弱而变得常见。本文提出一种潜在的新型机制，用于解释克鲁格国家公园非洲水牛（Syncerus caffer）种群中有害等位基因高频出现的现象：该机制由性别比抑制因子（sex-ratio suppressor）驱动，对这些等位基因产生正选择作用。我们此前的研究表明，四分之一的克鲁格水牛具有一种Y染色体分型（Y-chromosome profile）——尽管该分型与较低的体况相关，却能赋予个体相对繁殖优势，并通过性别比抑制因子得以稳定维持。显然，该性别比抑制因子可避免通常伴随性别比畸变出现的生育力降低。我们提出如下假说：这种与体况相关的繁殖优势，会提升对雄性体况产生负面影响的等位基因的适合度，进而引发这些等位基因的全基因组正选择。为验证该假说，我们利用17个常染色体微卫星标记（autosomal microsatellites）对459头水牛进行基因分型。通过将杂合度与体况进行关联分析（即杂合度-适合度相关性分析，heterozygosity-fitness correlations），我们发现大多数微卫星标记与两类基因相关：一类携带的有害等位基因频率升高，且无论性别如何均会对体况产生负面影响；另一类携带性拮抗等位基因（sexually antagonistic alleles），此类等位基因对雄性体况产生负面影响，却对雌性体况具有积极作用。等位基因渐变群（allele clines）以及性别比抑制因子携带者中纯合有害等位基因的相对高比例，分别印证了正选择作用以及该因子与Y染色体的直接关联。本研究采用全新的统计学方法分析杂合度-适合度相关性，首次在自然哺乳动物种群中证实了性拮抗基因的广泛存在。本研究不仅有助于理解性别比畸变因子及其抑制因子的进化与生态动力学，也为阐释有害等位基因与性拮抗等位基因的功能及其对种群生存力（population viability）的影响提供了重要启示。