Close inbreeding and low genetic diversity in Inner Asian human populations despite geographical exogamy

Open access Close inbreeding and low genetic diversity in Inner Asian human populations despite geographical exogamy, by Marchi et al. Scientific Reports (2018) 8:9397.

Abstract (emphasis mine):

When closely related individuals mate, they produce inbred offspring, which often have lower fitness than outbred ones. Geographical exogamy, by favouring matings between distant individuals, is thought to be an inbreeding avoidance mechanism; however, no data has clearly tested this prediction. Here, we took advantage of the diversity of matrimonial systems in humans to explore the impact of geographical exogamy on genetic diversity and inbreeding. We collected ethno-demographic data for 1,344 individuals in 16 populations from two Inner Asian cultural groups with contrasting dispersal behaviours (Turko-Mongols and Indo-Iranians) and genotyped genome-wide single nucleotide polymorphisms in 503 individuals. We estimated the population exogamy rate and confirmed the expected dispersal differences: Turko-Mongols are geographically more exogamous than Indo-Iranians. Unexpectedly, across populations, exogamy patterns correlated neither with the proportion of inbred individuals nor with their genetic diversity. Even more surprisingly, among Turko-Mongols, descendants from exogamous couples were significantly more inbred than descendants from endogamous couples, except for large distances (>40 km). Overall, 37% of the descendants from exogamous couples were closely inbred. This suggests that in Inner Asia, geographical exogamy is neither efficient in increasing genetic diversity nor in avoiding inbreeding, which might be due to kinship endogamy despite the occurrence of dispersal.

Interesting excerpts:

Two cultural groups, which matrimonial systems are reported to differ, coexist in Inner Asia: Turko-Mongols are described as mainly exogamous while Indo-Iranians are thought to be mainly endogamous45. However, it is not always clear if exogamy refers to clan (ethnic) or village (geographical) exogamy. Here, we used a dataset of 16 populations representing 11 different ethnic groups from both cultural groups and we quantified geographical exogamy rates and distances in each population. Using an empirical threshold of 4 km, we confirmed that matrimonial behaviours differ as described in the literature, even though we found some exceptions: three Turko-Mongol populations (out of 14) have less than 50% exogamy, whereas one Indo-Iranian population (out of four) has more than 50% exogamy.(…).

geographic-distance-turko-mongols-indo-iranian
Geographical distances between the birth places of couples in Turko-Mongols and Indo-Iranians. The geographical distances are plotted in log scale (km). Their densities are represented by population (dashed lines) or for the Indo-Iranian and Turko-Mongol groups (solid lines). We represented the average distances within couples per population using a Kernel’s density estimate implemented in R with a smoothing bandwidth of 0.2. See Supplementary Table 1B for population codes.

An additional important result of our study is that geographical distances are not negatively correlated with inbreeding, as could have been expected under an isolation-by-distance model65. Interestingly, a recent study based on a large genealogical dataset, collected across Western Europe and North America, and including birth places information, similarly found an absence of correlation between relatedness and the distance between couples, for the cohorts born before 185066. Our analyses within present-day Turko-Mongols reveal more specifically that the structure of the relationship between geographical distance and mating choice inbreeding is not linear, but rather tends to be bell-shaped, and thus cannot be correctly assessed with a single correlation test. Indeed, descendants from parents born 4 to 40 km apart are more inbred than descendants from endogamous couples (≤4 km) or from long-range exogamous ones (>40 km). As a consequence, close inbreeding exists despite geographical exogamy, and about a third of descendants from exogamous couples are inbred.

These results, in addition to those obtained by [Kaplanis et al. 2018]66, highlight the importance of using geographic distances rather than exogamy rates to characterize the impact of exogamy on inbreeding, as already described when studying patrilocality67. Indeed, when we compare mating choice inbreeding patterns for descendants from exogamous and endogamous couples defined for thresholds of 4, 10, 20 and 30 km, we find no significant differences (for number and total length of class C-ROHs and F-Median coefficient: MWU test p-values > 0.1). We only detect significantly lower values in descendants from exogamous couples for larger distances above 40 and 50 km (p-values < 0.03).

genetic-diversity-turko-mongol-indo-iranian
Genetic diversity (A) and inbreeding patterns (B,C) within populations. Grey lines in (B) represent inbreeding values corresponding to second-cousins and first-cousins. The grey line in (C) represents the homozygosity population baseline expected under panmixia. The number of samples per population is indicated between parentheses. See Supplementary Table 1B for population codes.

Our results also challenge the intuition that exogamy necessarily increases the genetic diversity within a population and therefore reduces drift inbreeding. Indeed, we found that Turko-Mongol populations have a lower genetic diversity (as measured by the mean haplotypic heterozygosity) and more intermediate ROHs associated with drift inbreeding than those of Indo-Iranians despite higher exogamous rates. (…)

Overall, this research sheds light on mating choice preferences: we showed that two thirds of partners that have not dispersed did mate with unrelated individuals, and that drift and mating choice inbreeding is variable, even among close-by populations. We also provide new insights into the relationship between dispersal and inbreeding in humans, based on genetic data, and demonstrate that geographical exogamy is not necessarily negatively associated with mating choice inbreeding, but rather can have a more complex non-linear relationship. Contrary to the common situation in many animals, this finding suggests that Inner Asian human populations who practise exogamy at small geographical scales might be focused on alliance strategies that result in kinship endogamy. (…)

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