Data from: Demography or selection on linked cultural traits or genes? Investigating the driver of low mtDNA diversity in the sperm whale using complementary mitochondrial and nuclear genome analyses

Mitochondrial DNA has been heavily utilized in phylogeography studies for several decades. However, underlying patterns of demography and phylogeography may be misrepresented due to coalescence stochasticity, selection, variation in mutation rates, and cultural hitchhiking (linkage of genetic variation to culturally transmitted traits affecting fitness). Cultural hitchhiking has been suggested as an explanation for low genetic diversity in species with strong social structures, counteracting even high mobility, abundance and limited barriers to dispersal. One such species is the sperm whale, which shows very limited phylogeographic structure and low mtDNA diversity despite a worldwide distribution and large population. Here, we use analyses of 175 globally distributed mitogenomes and three nuclear genomes to evaluate hypotheses of a population bottleneck/expansion versus a selective sweep due to cultural-hitchhiking or selection on mtDNA as the mechanism contributing to low worldwide mitochondrial diversity in sperm whales. In contrast to mtDNA control region (CR) data, mitogenome haplotypes are largely ocean-specific, with only one of 80 shared between the Atlantic and Pacific. Demographic analyses of nuclear genomes suggest low mtDNA diversity is consistent with a global reduction in population size that ended approximately 125,000 years ago, correlated with the Eemian interglacial. Phylogeographic analysis suggests that extant sperm whales descend from maternal lineages endemic to the Pacific during the period of reduced abundance, and have subsequently colonized the Atlantic several times. Results highlight the apparent impact of past climate change, and suggest selection and hitchhiking are not the sole processes responsible for low mtDNA diversity in this highly social species.

数十年来，线粒体DNA（mitochondrial DNA, mtDNA）一直被广泛应用于系统地理学研究。然而，由于溯祖随机性、自然选择、突变率差异以及文化搭车效应（即遗传变异与影响个体适合度的文化传承性状连锁）的存在，种群历史与系统地理学的潜在模式或遭误判。文化搭车效应曾被用以解释具有强社会结构的物种种群遗传多样性偏低的现象——即便这类物种具备高移动性、庞大种群规模与有限的扩散障碍，该效应仍可抵消这些有利条件。抹香鲸便是此类物种之一：尽管其全球广布且种群规模庞大，但其系统地理学结构极有限，线粒体DNA多样性亦偏低。本研究通过对175个全球分布的线粒体基因组与3个核基因组开展分析，旨在验证两种假说：一是种群瓶颈/扩张事件，二是由文化搭车效应或线粒体DNA选择驱动的选择性清除，以此阐明抹香鲸全球线粒体多样性偏低的成因。与线粒体DNA控制区（CR）数据不同，线粒体基因组单倍型大多具有海洋特异性，80个单倍型中仅1个在大西洋与太平洋间共享。核基因组的种群统计学分析显示，线粒体DNA多样性偏低与约12.5万年前结束的全球种群规模缩减事件相符，该事件与埃姆间冰期存在关联。系统地理学分析表明，现存抹香鲸源自丰度降低时期太平洋特有的母系谱系，随后多次向大西洋扩散定居。研究结果凸显了古气候变化的显著影响，并表明选择与搭车效应并非导致这一高度社会化物种种线粒体DNA多样性偏低的唯一过程。