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      A Bayesian Implementation of the Multispecies Coalescent Model with Introgression for Phylogenomic Analysis

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          Abstract

          Recent analyses suggest that cross-species gene flow or introgression is common in nature, especially during species divergences. Genomic sequence data can be used to infer introgression events and to estimate the timing and intensity of introgression, providing an important means to advance our understanding of the role of gene flow in speciation. Here, we implement the multispecies-coalescent-with-introgression model, an extension of the multispecies-coalescent model to incorporate introgression, in our Bayesian Markov chain Monte Carlo program Bpp. The multispecies-coalescent-with-introgression model accommodates deep coalescence (or incomplete lineage sorting) and introgression and provides a natural framework for inference using genomic sequence data. Computer simulation confirms the good statistical properties of the method, although hundreds or thousands of loci are typically needed to estimate introgression probabilities reliably. Reanalysis of data sets from the purple cone spruce confirms the hypothesis of homoploid hybrid speciation. We estimated the introgression probability using the genomic sequence data from six mosquito species in the Anopheles gambiae species complex, which varies considerably across the genome, likely driven by differential selection against introgressed alleles.

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          Most cited references45

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          Testing for ancient admixture between closely related populations.

          One enduring question in evolutionary biology is the extent of archaic admixture in the genomes of present-day populations. In this paper, we present a test for ancient admixture that exploits the asymmetry in the frequencies of the two nonconcordant gene trees in a three-population tree. This test was first applied to detect interbreeding between Neandertals and modern humans. We derive the analytic expectation of a test statistic, called the D statistic, which is sensitive to asymmetry under alternative demographic scenarios. We show that the D statistic is insensitive to some demographic assumptions such as ancestral population sizes and requires only the assumption that the ancestral populations were randomly mating. An important aspect of D statistics is that they can be used to detect archaic admixture even when no archaic sample is available. We explore the effect of sequencing error on the false-positive rate of the test for admixture, and we show how to estimate the proportion of archaic ancestry in the genomes of present-day populations. We also investigate a model of subdivision in ancestral populations that can result in D statistics that indicate recent admixture.
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            Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci.

            The effective population sizes of ancestral as well as modern species are important parameters in models of population genetics and human evolution. The commonly used method for estimating ancestral population sizes, based on counting mismatches between the species tree and the inferred gene trees, is highly biased as it ignores uncertainties in gene tree reconstruction. In this article, we develop a Bayes method for simultaneous estimation of the species divergence times and current and ancestral population sizes. The method uses DNA sequence data from multiple loci and extracts information about conflicts among gene tree topologies and coalescent times to estimate ancestral population sizes. The topology of the species tree is assumed known. A Markov chain Monte Carlo algorithm is implemented to integrate over uncertain gene trees and branch lengths (or coalescence times) at each locus as well as species divergence times. The method can handle any species tree and allows different numbers of sequences at different loci. We apply the method to published noncoding DNA sequences from the human and the great apes. There are strong correlations between posterior estimates of speciation times and ancestral population sizes. With the use of an informative prior for the human-chimpanzee divergence date, the population size of the common ancestor of the two species is estimated to be approximately 20,000, with a 95% credibility interval (8000, 40,000). Our estimates, however, are affected by model assumptions as well as data quality. We suggest that reliable estimates have yet to await more data and more realistic models.
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              Hybridization, introgression, and the nature of species boundaries.

              Species can be defined as populations that are diagnosably distinct, reproductively isolated, cohesive, or exclusive groups of organisms. Boundaries between species in sympatry are maintained by intrinsic barriers to gene exchange; these boundaries may not be uniform in space, in time, or across the genome. Here, we explore the nature of the species boundary, defined as the phenotypes/genes/genome regions that remain differentiated in the face of potential hybridization and introgression. We emphasize that species boundaries are semipermeable, with permeability (gene exchange) being a function of genome region. The early evidence for semipermeable species boundaries came from data on differential introgression in hybrid zones. This "genic view" of species was common in the hybrid zone literature even when few molecular markers were available to characterize genome-wide patterns of variation. Now, molecular tools allow detailed characterization of differentiation between diverging lineages and patterns of variation across natural hybrid zones, but the questions being asked by evolutionary biologists have remained much the same. Recent data (from DNA sequences and genotypes) reinforce earlier conclusions about the semipermeable nature of most species boundaries. However, debate persists over the nature and extent of genome divergence that accompanies speciation.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Mol Biol Evol
                Mol. Biol. Evol
                molbev
                Molecular Biology and Evolution
                Oxford University Press
                0737-4038
                1537-1719
                April 2020
                06 December 2019
                06 December 2019
                : 37
                : 4
                : 1211-1223
                Affiliations
                [1 ] Department of Genetics, Evolution and Environment, University College London , London, United Kingdom
                [2 ] Department of Evolution and Ecology, University of California , Davis, Davis, CA
                Author notes
                Corresponding author: E-mail: z.yang@ 123456ucl.ac.uk .
                Article
                msz296
                10.1093/molbev/msz296
                7086182
                31825513
                ea21e21f-783c-4fc5-a757-ab376185bb97
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 13
                Funding
                Funded by: Biotechnological and Biological Sciences Research Council;
                Award ID: BB/N000609/1
                Award ID: BB/P006493/1
                Funded by: BBSRC equipment grant;
                Award ID: BB/R01356X/1
                Categories
                Methods

                Molecular biology
                bayesian inference,bpp,introgression,multispecies coalescent with introgression,msci,mcmc

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