Human inbreeding has decreased in time through the Holocene

Abstract

SummaryThe history of human inbreeding is controversial. The development of sedentary agricultural societies may have had opposite influences on inbreeding levels. On the one hand, agriculture and food surplus may have diminished inbreeding by increasing population sizes and lowering endogamy, i.e. inbreeding due to population isolation. On the other hand, increased sedentism, as well as the advent of private property may have promoted inbreeding through the emergence of consanguineous marriage customs or via ethnic and caste endogamy. The net impact is unknown, and to date, no systematic study on the temporal frequency of inbreeding in human societies has been conducted. Here we present a new approach for reliable estimation of runs of homozygosity (ROH) in genomes with ≥3x mean coverage across >1 million SNPs, and apply this to 440 ancient Eurasian genomes from the last 15,000 years. We show that the frequency of inbreeding, as measured by ROH, has decreased over time. The strongest effect is associated with the Neolithic transition, but the trend has since continued, indicating a population size effect on inbreeding prevalence. We further show that most inbreeding in our historical sample can be attributed to endogamy, although singular cases of high consanguinity can also be found in the archaeogenomic record.HighlightsA study of 440 ancient genomes shows inbreeding decreased over time.The decrease appears linked with population size increase due to farming.Extreme consanguineous matings did occur among farmers, but rarely.

Demogenomic modeling of the timing and the processes of early European farmers differentiation

“…Compared to the other samples, the HG genomes, and in particular Bichon and SF12, show a larger proportion of short (2-10Mb) Runs of Homozygosity (ROHs, Fig. 2c ), in keeping with previous results 17,28,29 . This is indicative of higher levels of remote inbreeding within European HGs, likely due to smaller population sizes as corroborated by MSMC2 analyses ( Fig.…”

“…2C). Contrary to previous interpretations (25,31), HGs are generally found to have larger population sizes than contemporary early farmer populations (Fig. 3A) which explains why they show close genetic affinities on the MDS (Fig.…”

“…2D, Fig. S20A) (24) indicative of remote inbreeding within European HGs and thought to be due to their small population size (25), in line with MSMC2 analyses (Fig. S25).…”

A genomic snapshot of demographic and cultural dynamism in Upper Mesopotamia during the Neolithic Transition

“…As reported earlier ( 8, 12, 21, 23 ), Aşıklı, Boncuklu, and Caucasus pre-Neolithic genomes carried large numbers of ROH, indicative of small population size. Certain Neolithic genomes (e.g., WC1, Ash128) also showed a “right-shift” when plotting the number versus sum of ROHs, indicative of recent inbreeding ( 34 ) (Fig. 5B-C).…”

“…We performed linear regression using short ROH (4-8 cM) in present-day genomes to create a baseline that represents solely drift with no recent inbreeding. Right-shift from the baseline indicates that parents of this individual could be close-kin, whereas individuals that are around the baseline, and also have a relatively high number of ROH come from a population with potentially low N e (effective population size) ( 34 ). We filtered out ROHs <4 cM following the original hapROH publication which suggested that the method can detect ROH >4 cM ( 33 ).…”