The Spatial Mixing of Genomes in Secondary Contact Zones

Abstract

Recent genomic studies have highlighted the important role of admixture in shaping genome-wide patterns of diversity. Past admixture leaves a population genomic signature of linkage disequilibrium (LD), reflecting the mixing of parental chromosomes by segregation and recombination. These patterns of LD can be used to infer the timing of admixture, but the results of inference can depend strongly on the assumed demographic model. Here, we introduce a theoretical framework for modeling patterns of LD in a geographic contact zone where two differentiated populations have come into contact and are mixing by diffusive local migration. Assuming that this secondary contact is recent enough that genetic drift can be ignored, we derive expressions for the expected LD and admixture tract lengths across geographic space as a function of the age of the contact zone and the dispersal distance of individuals. We develop an approach to infer age of contact zones, using population genomic data from multiple spatially sampled populations by fitting our model to the decay of LD with recombination distance. To demonstrate an application of our model, we use our approach to explore the fit of a geographic contact zone model to three human genomic data sets from populations in Indonesia, Central Asia, and India and compare our results to inference under different demographic models. We obtain substantially different results from those of the commonly used model of panmictic admixture, highlighting the sensitivity of admixture timing results to the choice of demographic model. KEYWORDS contact zones; admixture; linkage disequilibrium P OPULATIONS frequently undergo periods of relative isolation that are followed by secondary contact. During isolation, the evolutionary processes of genetic drift, mutation, and selection act to differentiate populations at many markers throughout the genome. When these populations come back into contact, the restoration of gene flow generates admixed populations, which start as an assemblage of differentiated parental genomes that are broken up every generation by segregation and recombination between chromosomes.Under this process, linked alleles of the same ancestry will tend to be co-inherited until separated by recombination. Because the parental populations are differentiated with respect to each other, this co-inheritance leads to a nonrandom association of alleles, referred to as linkage disequilibrium (LD). This admixture-induced LD (or admixture LD) is the resulting covariance between loci and initially extends over a much larger genomic scale than LD does in either parental population and is a signature of relatively recent admixture (Cavalli-Sforza and Bodmer 1971;Chakraborty and Weiss 1988). One can also think of this signature as the persistence of parental haplotypes in admixed populations that, rather than being measured directly, is measured as the extent of cooccurrence along a chromosome of alleles that are diagnostic of parental origin. Recombination acts every generation to...

Signatures of hybridization and speciation in genomic patterns of ancestry*

“…Geographic clines (Szymura and Barton 1986;Barton and Hewitt 1989;Mallet et al 1990;Barton and Gale 1993;Porter et al 1997) and genomic clines (Szymura and Barton 1986;Buerkle 2009, 2011;Fitzpatrick 2013) enable inferences about speciation from genomic data in hybrid zones. We extended the idea that analyzing ancestry switching across genomes is a useful and complementary strategy (Barton 1983;Baird 1995Baird , 2006Ungerer et al 1998;Buerkle and Rieseberg 2008;Sedghifar et al 2015Sedghifar et al , 2016.…”

“…Since junctions are inherited like point mutations (Baird 2006), we might expect a positive correlation between the age of a junction and its frequency. Based on results from Sedghifar et al (2015Sedghifar et al ( , 2016, modeling the consequences of selection for geographic junction patterns is likely to be another fertile direction. Furthermore, the extent to which BDMIs can block gene flow between species remains a topic worthy of attention (Gavrilets 1997;Bank et al 2012;Lindtke and Buerkle 2015).…”

“…The lengths of ancestry tracts are directly connected to the number of generations of hybridization. This observation raises the prospect of using a "recombination clock" to characterize the timescale of hybridization (Baird 1995;Pool and Nielsen 2009;Sedghifar et al 2015), an approach that has been successfully applied in sunflowers (Ungerer et al 1998;Buerkle and Rieseberg 2008) and cichlids (Meier et al 2017). Reproductive isolation conferred by heterozygote disadvantage is predicted to maintain longer ancestry tracts under some conditions (Barton 1983;Baird 1995;Sedghifar et al 2016).…”

“…Reproductive isolation conferred by heterozygote disadvantage is predicted to maintain longer ancestry tracts under some conditions (Barton 1983;Baird 1995;Sedghifar et al 2016). The interaction between gene flow and recombination in hybrid zones is expected to produce geographic gradients in ancestry tracts (Sedghifar et al 2015).…”

Differential introgression across newt hybrid zones: Evidence from replicated transects

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