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（hitchhiking）或选择约束（selective constraints）减弱而变得常见。本文提出一种全新的潜在机制，用以解释克鲁格国家公园内非洲水牛（Syncerus caffer）种群中有害等位基因频率居高不下的现象——该机制由性比抑制因子（sex-ratio suppressor）最终驱动，通过对这些等位基因的正选择（positive selection）实现。此前我们已证实，每4只克鲁格水牛中便有1只携带特定Y染色体分型：尽管该分型与较低的体况相关，却能赋予个体相对的繁殖优势，且该分型可通过性比抑制因子稳定维持。显然，该性比抑制因子可阻止性比畸变通常伴随的生育力下降。我们据此提出假说：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（fitness），进而引发这些等位基因在全基因组范围内的正选择。为验证该假说，我们利用17个常染色体微卫星（autosomal microsatellites）对459只水牛进行了基因分型。通过将杂合性（heterozygosity）与体况进行关联分析（即杂合性-适合度相关性分析，heterozygosity-fitness correlations），我们发现大多数微卫星可归为两类基因之一：一类携带频率升高的有害等位基因，此类等位基因无论性别如何均会对体况产生负面影响；另一类携带频率升高的性拮抗等位基因（sexually antagonistic alleles），此类等位基因对雄性体况存在负面影响，却能提升雌性体况。等位基因梯度（allele clines）以及性比抑制因子携带者中纯合有害等位基因的数量相对偏高，分别印证了正选择以及与Y染色体性比抑制因子的直接关联。本研究采用新型统计技术开展杂合性-适合度相关性分析，首次证实了自然哺乳动物种群中性拮抗基因的普遍性。本研究不仅有助于我们理解性比畸变因子与抑制因子的进化及生态动态，也能加深我们对有害等位基因与性拮抗等位基因的功能、以及它们对种群生存力（population viability）的影响的认知。