A historical-genetic reconstruction of human extra-pair paternity

Paternity testing using genetic markers has shown that extra-pair paternity (EPP) is common in many pair-bonded species. Evolutionary theory and empirical data show that extra-pair copulations can increase the fitness of males as well as females. This can carry a significant fitness cost for the social father, who then invests in rearing offspring that biologically are not his own. In human populations, the incidence and correlates of extra-pair paternity remain highly contentious. Here, we use a population-level genetic genealogy approach to reconstruct spatiotemporal patterns in human EPP rates. Using patrilineal genealogies from the Low Countries spanning a period of over 500 years and Y-chromosomal genotyping of living descendants, our analysis reveals that historical EPP rates, while low overall, were strongly impacted by socioeconomic and demographic factors. Specifically, we observe that estimated EPP rates among married couples varied by more than an order of magnitude, from 0.4% to 5.9%, and peaked among families with a low socioeconomic background living in densely populated cities of the late 19th century. Our results support theoretical predictions that social context can strongly affect the outcomes of sexual conflict in human populations by modulating the incentives and opportunities for engaging in extra-pair relationships. These findings show how contemporary genetic data combined with in-depth genealogies open up a new window on the sexual behaviour of our ancestors.

借助遗传标记开展的父权鉴定研究显示，婚外父权（extra-pair paternity, EPP）在诸多配对结合的物种中普遍存在。进化理论与实证数据均表明，婚外交配既能提升雄性的进化适合度，也能提升雌性的进化适合度。这会给社会父亲带来显著的适合度成本——后者需投入资源抚育在生物学上并非自身亲生的后代。在人类群体中，婚外父权的发生率及其相关影响因素仍存在极大争议。本研究借助群体水平的遗传谱系学方法，重构了人类婚外父权率的时空分布模式。我们使用了低地国家（Low Countries）跨度超500年的父系谱系资料，以及当代后裔的Y染色体基因分型数据，分析显示：尽管历史上的婚外父权率整体偏低，但仍受社会经济与人口统计学因素的强烈影响。具体而言，我们观测到已婚夫妇间的估算婚外父权率差异超过一个数量级，介于0.4%至5.9%之间，并在19世纪后期居住于人口稠密城市的低社会经济地位家庭中达到峰值。本研究结果支持相关理论预测：社会背景可通过调节个体发生婚外关系的动机与机会，强烈影响人类群体中的性冲突结局。这些研究成果展示了当代遗传数据与深度谱系资料相结合的方式，为探究我们祖先的性行为模式开辟了全新视角。