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      High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment

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          Abstract

          Studying recent adaptive radiations in isolated insular systems avoids complicating causal events and thus may offer clearer insight into mechanisms generating biological diversity. Here, we investigate evolutionary relationships and genomic differentiation within the recent radiation of Alcolapia cichlid fish that exhibit extensive phenotypic diversification, and which are confined to the extreme soda lakes Magadi and Natron in East Africa. We generated an extensive RAD data set of 96 individuals from multiple sampling sites and found evidence for genetic admixture between species within Lake Natron, with the highest levels of admixture between sympatric populations of the most recently diverged species. Despite considerable environmental separation, populations within Lake Natron do not exhibit isolation by distance, indicating panmixia within the lake, although individuals within lineages clustered by population in phylogenomic analysis. Our results indicate exceptionally low genetic differentiation across the radiation despite considerable phenotypic trophic variation, supporting previous findings from smaller data sets; however, with the increased power of densely sampled SNPs, we identify genomic peaks of differentiation ( F ST outliers) between Alcolapia species. While evidence of ongoing gene flow and interspecies hybridization in certain populations suggests that Alcolapia species are incompletely reproductively isolated, the identification of outlier SNPs under diversifying selection indicates the radiation is undergoing adaptive divergence.

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          Neighbor-net: an agglomerative method for the construction of phylogenetic networks.

          We present Neighbor-Net, a distance based method for constructing phylogenetic networks that is based on the Neighbor-Joining (NJ) algorithm of Saitou and Nei. Neighbor-Net provides a snapshot of the data that can guide more detailed analysis. Unlike split decomposition, Neighbor-Net scales well and can quickly produce detailed and informative networks for several hundred taxa. We illustrate the method by reanalyzing three published data sets: a collection of 110 highly recombinant Salmonella multi-locus sequence typing sequences, the 135 "African Eve" human mitochondrial sequences published by Vigilant et al., and a collection of 12 Archeal chaperonin sequences demonstrating strong evidence for gene conversion. Neighbor-Net is available as part of the SplitsTree4 software package.
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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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              Divergent selection and heterogeneous genomic divergence.

              Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome-wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) 'outlier loci' with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs ['isolation by adaptation' (IBA)]. The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5-10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.
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                Author and article information

                Journal
                Mol Ecol
                Mol. Ecol
                10.1111/(ISSN)1365-294X
                MEC
                Molecular Ecology
                John Wiley and Sons Inc. (Hoboken )
                0962-1083
                1365-294X
                July 2015
                19 June 2015
                : 24
                : 13 ( doiID: 10.1111/mec.2015.24.issue-13 )
                : 3421-3440
                Affiliations
                [ 1 ] Department of Genetics Evolution and EnvironmentUniversity College London London WC1E 6BTUK
                [ 2 ] Department of BiologyUniversity of York York YO10 5DDUK
                [ 3 ]Naturhistorisches Museum der Burgergemeinde Bern Bernastrasse 15 Bern 3005Switzerland
                [ 4 ] Edinburgh Genomics Ashworth LaboratoriesThe University of Edinburgh Edinburgh EH9 3FLUK
                Author notes
                [*] [* ]Correspondence: Antonia G. P. Ford, Fax: +44 (0)207 6797193; E‐mail: a.ford.11@ 123456ucl.ac.uk
                Article
                MEC13247
                10.1111/mec.13247
                4973668
                25997156
                7707e31e-81bc-4a9e-9b96-5281a6422ff9
                © 2015 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Page count
                Pages: 20
                Product
                Funding
                Funded by: BBSRC/NERC SynTax
                Funded by: UCL Graduate Scholarship
                Funded by: Graduate School Research Project Fund Award
                Funded by: Genetics Society
                Funded by: Percy Sladen Memorial Fund
                Categories
                Original Article
                ORIGINAL ARTICLES
                Speciation and Hybridization
                Custom metadata
                2.0
                mec13247
                July 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:04.08.2016

                Ecology
                adaptive radiation,admixture,alcolapia,cichlid,hybridization,lake magadi,lake natron,oreochromis,rad
                Ecology
                adaptive radiation, admixture, alcolapia, cichlid, hybridization, lake magadi, lake natron, oreochromis, rad

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