Laboratory for Animal Social Evolution and Recognition, Department of Neurobiology and Behavior, Cornell University, Ithaca, New York, USA.
Department of Biology, University of Missouri St. Louis, St. Louis, Missouri, USA.
Mol Ecol. 2023 Aug;32(16):4546-4556. doi: 10.1111/mec.17057. Epub 2023 Jun 23.
Deleterious variants are selected against but can linger in populations at low frequencies for long periods of time, decreasing fitness and contributing to disease burden in humans and other species. Deleterious variants occur at low frequency but distinguishing deleterious variants from low-frequency neutral variation is challenging based on population genomics data alone. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesised that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females when deleterious variants are recessive, resulting in more efficient purging of deleterious mutations in males. Therefore, comparisons of the differences between haploid and diploid genomes from the same population may be a useful method for inferring rare deleterious variants. This study provides the first formal test of this hypothesis. Using wild populations of Northern paper wasps (Polistes fuscatus), we find that males have fewer missense and nonsense variants per generation than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense variants and these differences lead to a lower mutational load in males than females. Based on these data we infer that many highly deleterious mutations are segregating in the paper wasp population. Stronger selection against deleterious alleles in haploid males may have implications for adaptation in other haplodiploid insects and provides evidence that wild populations harbour abundant deleterious variants.
有害变异体受到选择的压力，但可以在低频率下在种群中长时间存在，降低了适应度，并导致人类和其他物种的疾病负担增加。有害变体的频率较低，但仅根据群体基因组学数据区分有害变体和低频中性变异具有挑战性。因此，我们对野生种群中有害变体的数量和身份知之甚少。对于单倍型二倍体物种，有人假设有害等位基因将在雄性单倍体中直接受到选择的影响，但当有害变体为隐性时，在雌性二倍体中选择可能被掩盖，从而导致雄性中有害突变的清除效率更高。因此，比较同一群体中单倍体和二倍体基因组之间的差异可能是推断稀有有害变体的有用方法。本研究首次对这一假设进行了正式测试。通过对北方纸巢蜂（Polistes fuscatus）的野生种群进行研究，我们发现雄性每个世代的错义和无义变异数量比来自同一种群的雌性要少。稀有错义和无义变异的等位基因频率差异尤其明显，这些差异导致雄性的突变负荷低于雌性。根据这些数据，我们推断出许多高度有害的突变在纸巢蜂种群中存在。在雄性单倍体中对有害等位基因的更强选择可能对其他单倍型二倍体昆虫的适应有影响，并提供了野生种群中存在大量有害变体的证据。
