Resource Ecology Group, Wageningen University, Wageningen, The Netherlands.
Department of Zoology & Entomology, Mammal Research Institute, University of Pretoria, Hatfield, South Africa.
PLoS One. 2019 Sep 4;14(9):e0221168. doi: 10.1371/journal.pone.0221168. eCollection 2019.
Bovine tuberculosis (BTB) is endemic to the African buffalo (Syncerus caffer) of Hluhluwe-iMfolozi Park (HiP) and Kruger National Park, South Africa. In HiP, the disease has been actively managed since 1999 through a test-and-cull procedure targeting BTB-positive buffalo. Prior studies in Kruger showed associations between microsatellite alleles, BTB and body condition. A sex chromosomal meiotic drive, a form of natural gene drive, was hypothesized to be ultimately responsible. These associations indicate high-frequency occurrence of two types of male-deleterious alleles (or multiple-allele haplotypes). One type negatively affects body condition and BTB resistance in both sexes. The other type has sexually antagonistic effects: negative in males but positive in females. Here, we investigate whether a similar gene drive system is present in HiP buffalo, using 17 autosomal microsatellites and microsatellite-derived Y-chromosomal haplotypes from 401 individuals, culled in 2002-2004. We show that the association between autosomal microsatellite alleles and BTB susceptibility detected in Kruger, is also present in HiP. Further, Y-haplotype frequency dynamics indicated that a sex chromosomal meiotic drive also occurred in HiP. BTB was associated with negative selection of male-deleterious alleles in HiP, unlike positive selection in Kruger. Birth sex ratios were female-biased. We attribute negative selection and female-biased sex ratios in HiP to the absence of a Y-chromosomal sex-ratio distorter. This distorter has been hypothesized to contribute to positive selection of male-deleterious alleles and male-biased birth sex ratios in Kruger. As previously shown in Kruger, microsatellite alleles were only associated with male-deleterious effects in individuals born after wet pre-birth years; a phenomenon attributed to epigenetic modification. We identified two additional allele types: male-specific deleterious and beneficial alleles, with no discernible effect on females. Finally, we discuss how our findings may be used for breeding disease-free buffalo and implementing BTB test-and-cull programs.
非洲野牛（Syncerus caffer）是南非赫卢赫卢韦-伊姆福洛兹公园（HiP）和克鲁格国家公园的地方性牛结核病（BTB）宿主。自 1999 年以来，HiP 通过针对 BTB 阳性野牛的测试和淘汰程序积极管理该疾病。先前在克鲁格的研究表明，微卫星等位基因、BTB 和身体状况之间存在关联。假设性染色体减数分裂驱动，一种自然基因驱动形式，是最终负责的原因。这些关联表明两种类型的雄性有害等位基因（或多等位基因单倍型）高频发生。一种类型对两性的身体状况和 BTB 抵抗力都有负面影响。另一种类型具有性拮抗作用：在雄性中为负，在雌性中为正。在这里，我们使用 17 个常染色体微卫星和 2002-2004 年间淘汰的 401 只个体的微卫星衍生 Y 染色体单倍型，调查 HiP 野牛中是否存在类似的基因驱动系统。我们表明，在克鲁格检测到的常染色体微卫星等位基因与 BTB 易感性之间的关联也存在于 HiP 中。此外，Y 染色体单倍型频率动态表明，减数分裂驱动也发生在 HiP 中。BTB 与 HiP 中雄性有害等位基因的负选择有关，而与克鲁格中的正选择相反。出生性别比偏向雌性。我们将 HiP 中的负选择和雌性偏向性别比归因于 Y 染色体性别比例扰乱因子的缺失。据推测，这种扰乱因子有助于克鲁格雄性有害等位基因的正选择和雄性偏向的出生性别比。如前所述，在克鲁格，只有在出生前潮湿年份出生的个体中，微卫星等位基因才与雄性有害影响相关联；这一现象归因于表观遗传修饰。我们确定了另外两种等位基因类型：雄性特异性有害和有益等位基因，对雌性没有明显影响。最后，我们讨论了我们的发现如何用于培育无病野牛和实施 BTB 测试和淘汰计划。
