Multiple episodes of interbreeding between Neanderthal and modern humans

Abstract

Neandertals and anatomically modern humans overlapped geographically for a period of over 30,000 years following human migration out of Africa. During this period, Neandertals and humans interbred, as evidenced by Neandertal portions of the genome carried by non-African individuals today. A key observation is that the proportion of Neandertal ancestry is ~12–20% higher in East Asian individuals relative to European individuals. Here, we explore various demographic models that could explain this observation. These include distinguishing between a single admixture event and multiple Neandertal contributions to either population, and the hypothesis that reduced Neandertal ancestry in modern Europeans resulted from more recent admixture with a ghost population that lacked a Neandertal ancestry component (the “dilution” hypothesis). In order to summarize the asymmetric pattern of Neandertal allele frequencies, we compile the joint fragment frequency spectrum (FFS) of European and East Asian Neandertal fragments and compare it to both analytical theory and data simulated under various models of admixture. Using maximum likelihood and machine learning, we found that a simple model of a single admixture does not fit the empirical data and instead favor a model of multiple episodes of gene flow into both European and East Asian populations. These findings indicate more long-term, complex interaction between humans and Neandertals than previously appreciated.

Models of archaic admixture and recent history from two-locus statistics

“…Many human lineages coexisted on the African continent, possibly until quite recently (Rightmire, 2009;Harvati et al, 2011;Berger et al, 2017), and genetic evidence points to a history of archaic admixture or deep structure across many modern African populations (Hammer et al, 2011;Lachance et al, 2012;Hsieh et al, 2016;Skoglund et al, 2017;Durvasula and Sankararaman, 2018;Hey et al, 2018). It is likely that modern humans have met and mixed with diverged lineages many times through history, rather than receiving just a single pulse of migrants (Browning et al, 2018;Villanea and Schraiber, 2019). We chose to model the mixing of archaic and modern human branches as continuous and symmetric (Kuhlwilm et al, 2016), parameterizing the migration rate between these branches and the times that migration began and ended.…”

Genomic determinants of speciation

“…However, modern genomic studies of animals (and human) revealed profound gene flow (introgression) between distinct species, blurring the boundaries between species. This relatively new concept suggests that the reproductive barrier between species, especially sister species, is frequently incomplete (Fontaine et al 2015; Heliconius Genome Consortium 2012; Villanea and Schraiber 2019). The perceived distinctness between animals recognized as different species, despite continuing gene flow between them (Mallet et al 2016), dazzled many biologists.…”

An amphibian species pushed out of Britain by a moving hybrid zone

“…One difference may be that leaky replacement implies that introgressed alleles increase the fitness of the invading species (as in adaptive introgression: Hedrick, ; Pardo‐Diaz et al, ; Racimo, Sankararaman, Nielsen, & Huerta‐Sánchez, ), but the consulted literature is not explicit at this point. In spite of a long history of investigation, considerable debate revolves around whether Neanderthals became extinct because of climate change or competition with anatomically modern humans (Banks et al, ; Benito et al, ; Gilpin, Feldman, & Aoki, ; Kolodny & Feldman, ; Melchionna et al, ) and the degree to which they hybridized (Currat & Excoffier, ; Neves & Serva, ; Villanea & Schraiber, ).…”

“…The inferred species transition that was labelled as "leaky replacement" (Pääbo, 2015; see also Gibbons, 2011), parallels that of a moving hybrid zone leaving a genetic footprint. One difference may be that leaky replacement implies that introgressed alleles increase the fitness of the invading (Banks et al, 2008;Benito et al, 2017;Gilpin, Feldman, & Aoki, 2016;Kolodny & Feldman, 2017;Melchionna et al, 2018) and the degree to which they hybridized (Currat & Excoffier, 2004;Neves & Serva, 2012;Villanea & Schraiber, 2019).…”