Among nonhuman species, social monogamy is rarely accompanied by complete fidelity. Evolutionary theory predicts that the rate of extrapair paternity (EPP) should vary according to socioecological conditions. In humans, however, geneticists contend that EPP is negligible and relatively invariable. This conclusion is based on a limited set of studies, almost all of which describe European-descent groups. Using a novel, double-blind method designed in collaboration with a community of Himba pastoralists, we find that the rate of EPP in this population is 48%, with 70% of couples having at least one EPP child. Both men and women were very accurate at detecting cases of EPP. These data suggest that the range of variation in EPP across human populations is substantially greater than previously thought. We further show that a high rate of EPP can be accompanied by high paternity confidence, which highlights the importance of disaggregating EPP from the notion of "cuckoldry."

Recessive alleles have been shown to directly affect both human Mendelian disease phenotypes and complex traits like height. Pedigree studies also suggest that consanguinity results in increased childhood mortality and adverse health phenotypes, presumably through penetrance of recessive mutations. Here, we test whether the accumulation of homozygous, recessive alleles decreases reproductive success in a human population. We address this question among the Namibian Himba, an endogamous agro-pastoralist population, who until very recently practiced natural fertility. Using a sample of 681 individuals, we show that Himba exhibit elevated levels of "inbreeding", calculated as the fraction of the genome in runs of homozygosity (FROH). Many individuals contain multiple long segments of ROH in their genomes, indicating that their parents had high kinship coefficients. However, we did not find evidence that this is explained by first-cousin consanguinity, despite a reported social preference for cross-cousin marriages. Rather, we show that elevated haplotype sharing in the Himba is due to a bottleneck, likely in the past 60 generations. We test whether increased recessive mutation load results in observed fitness consequences by assessing the effects of FROH on completed fertility in a cohort of post-reproductive women (n=69). We find that higher FROH is significantly associated with lower fertility among women who have had at least one child (p<0.006). Our data suggest a multi-locus genetic effect on fitness driven by the expression of deleterious recessive alleles, especially those in long ROH. However, these effects are not the result of consanguinity but rather elevated background identity by descent.

Objectives: Height is a complex, highly heritable polygenic trait subject to both genetic composition and environmental influences. Recent studies suggest that a large proportion of height heritability is determined by the cumulative effect of many low allele frequency variants across the genome. Previous research has also identified an inverse relationship between height and runs of homozygosity (ROH); however, this has yet to be examined within African populations. We aim to identify this association within the Himba, an endogamous Namibian population who are recently bottlenecked, resulting in elevated haplotype sharing and increased homozygosity.Materials and Methods: Here, we calculate the fraction of the genome composed of long runs of homozygosity (F ROH ) in a sample of 245 adults and use mixed effects models to assess its effect on height.Results: We find that Himba adults exhibit increased homozygosity. However, in contrast to previous studies in other populations, we do not find a significant effect of F ROH on height within the Himba. We further estimated heritability of height, noting both an enrichment of distant relatives and greater developmental homogeneity across households; we find that h 2 g ¼ 0:59 (SE ± 0.146), comparable to estimates reported in Europeans.Discussion: Our results may be due to other environmental variables we were not able to include, measurement error, or low statistical power, but may also imply that phenotypic expression resulting from increased homozygosity may vary from population to population.

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