A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

Abstract

Admixture-the mixing of genomes from divergent populations-is increasingly appreciated as a central process in evolution. To characterize and quantify patterns of admixture across the genome, a number of methods have been developed for local ancestry inference. However, existing approaches have a number of shortcomings. First, all local ancestry inference methods require some prior assumption about the expected ancestry tract lengths. Second, existing methods generally require genotypes, which is not feasible to obtain for many nextgeneration sequencing projects. Third, many methods assume samples are diploid, however a wide variety of sequencing applications will fail to meet this assumption. To address these issues, we introduce a novel hidden Markov model for estimating local ancestry that models the read pileup data, rather than genotypes, is generalized to arbitrary ploidy, and can estimate the time since admixture during local ancestry inference. We demonstrate that our method can simultaneously estimate the time since admixture and local ancestry with good accuracy, and that it performs well on samples of high ploidy-i.e. 100 or more chromosomes. As this method is very general, we expect it will be useful for local ancestry inference in a wider variety of populations than what previously has been possible. We then applied our method to pooled sequencing data derived from populations of Drosophila melanogaster on an ancestry cline on the east coast of North America. We find that regions of local recombination rates are negatively correlated with the proportion of African ancestry, suggesting that selection against foreign ancestry is the least efficient in low recombination regions. Finally we show that clinal outlier loci are enriched for genes associated with gene regulatory functions, consistent with a role of regulatory evolution in ecological adaptation of admixed D. melanogaster populations. Our results illustrate the potential of local ancestry inference for elucidating fundamental evolutionary processes. Data Availability Statement:No novel data were produced for this work. Short read data analyzed in this work are all available through the NCBI short read trace archive under project accession number PRJNA256231.Funding: RCD was supported by a Chancellor's Postdoctoral Fellowship during this work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author SummaryWhen divergent populations hybridize, their offspring obtain portions of their genomes from each parent population. Although the average ancestry proportion in each descendant is equal to the proportion of ancestors from each of the ancestral populations, the contribution of each ancestry type is variable across the genome. Estimating local ancestry within admixed individuals is a fundamental goal for evolutionary genetics, and here we develop a method for doing this that circumvents many of the problems associated with existing methods. Briefly, our method c...

Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

“…It is also likely that selection acts to maintain parental gene combinations against recombination (Bierne et al, ; Simon et al, ). Both effects, gene flow and selection, tend to bias the date estimates towards more recent times (Corbett‐Detig & Nielsen, ). A precise estimation of the admixture event will require a recombination map in mussels and the distribution of ancestry track lengths along the genome of admixed individuals.…”

Signatures of hybridization and speciation in genomic patterns of ancestry*

“…Probabilistic methods that reconstruct ancestry across the genome in admixed populations offer potential solutions (Wegmann et al. ; Corbett‐Detig and Nielsen ), but their performance in hybrid zones should be evaluated. It is worth emphasizing that alternative frameworks for analyzing hybrid zone data (including geographic clines and genomic clines) usually assume that species ancestry can be reconstructed from variant genotypes.…”

The spatial scale of dispersal revealed by admixture tracts

“…Although methodological improvements will be needed to better account for ancient migrations, the proposed approach provides a roadmap to generate valuable information on a conservation‐relevant timescale and is already well suited for species with relatively recent admixture histories. The development of new methods that simultaneously estimate local ancestry and the time since admixture (Corbett‐Detig & Nielsen, ) should further accelerate the interest for this kind of approach. This is especially true for species in which direct measures of dispersal are not applicable and the neutral migration–drift balance is not informative or simply does not exist, which is the case for many marine species.…”

“…Phased sequence data are even not necessary with some methods that only require the physical (Baran et al, ) or genetic (Guan, ) position of variants to identify ancestry blocks (Baran et al, ; Guan, ). Recently, a new method has also been developed to perform LAI directly from reads pileup data in population samples with arbitrary ploidy (Corbett‐Detig & Nielsen, ). Therefore, there is a good potential for using the length of tracts to date admixture, including with reduced‐representation sequencing data that still represent the most common type of data used in population genomic studies.…”

“…Furthermore, we use simulations to evaluate the robustness and the generality of this strategy to different admixture histories and sample sizes. With the development of new LAI methods to estimate the length distribution of admixture tracts (Corbett‐Detig & Nielsen, ; Medina, Thornlow, Nielsen, & Corbett‐Detig, ), we expect that quantitative assessments of dispersal will be obtained in several other species, which may help to resolve a long‐standing issue in conservation biology.…”