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

Abstract

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.

Figure 1

Geographical locations of the 16 Inner Asian populations sampled for this study. On this map generated from maps and mapdata R packages, the populations are coloured based on their linguistic affiliation, which also correlates with their matrimonial system. Note that the Kel population is composed of Northern Asian Kyrgyz from two different locations, and that Kaz and Uzb, as well as Akz and Tlg, were sampled at the same location, respectively. UZB.: Uzbekistan, KYR.: Kyrgyzstan, TUR.: Turkmenistan, TAJ.: Tajikistan, AFG.: Afghanistan, PAK.: Pakistan. See Supplementary Table 1B for population codes.

Figure 2

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.

Figure 3

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.

Figure 4

Parental couple distances and close inbreeding patterns for descendants from Turko-Mongols. For each of three estimators of inbreeding, we show in red the median value for four different classes of parental distances (<4 km, 4–20 km, 20–40 km and <40 km) as well as confidence intervals at 25% and 75%. The results of a MWU test comparing the <4 km class to all three others is shown below the plot.