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      Ancient hybridization fuels rapid cichlid fish adaptive radiations

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          Abstract

          Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region encompass >700 diverse species that all evolved in the last 150,000 years. How this ‘Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation.

          Abstract

          Cichlids underwent a rapid diversification in the Lake Victoria region, expanding to more than 700 species within 150,000 years. Here, Meier and colleagues show that an ancient hybridization between two divergent cichlid lineages generated high genetic diversity that facilitated the rapid radiation.

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          Most cited references44

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            Gene Trees in Species Trees

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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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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                10 February 2017
                2017
                : 8
                : 14363
                Affiliations
                [1 ]Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern , 3012 Bern, Switzerland
                [2 ]Department of Fish Ecology and Evolution, Centre for Ecology, Evolution & Biogeochemistry, Eawag: Swiss Federal Institute of Aquatic Science and Technology , 6047 Kastanienbaum, Switzerland
                [3 ]Computational and Molecular Population Genetics Lab, Institute of Ecology and Evolution, University of Bern , 3012 Bern, Switzerland
                [4 ]Biodiversity Institute & Department of Botany, University of Wyoming , Laramie Wyoming 82071, USA
                [5 ]Swiss Institute of Bioinformatics , 1015 Lausanne, Switzerland
                Author notes
                Author information
                http://orcid.org/0000-0002-0241-1685
                http://orcid.org/0000-0002-7507-6494
                http://orcid.org/0000-0001-6598-1434
                Article
                ncomms14363
                10.1038/ncomms14363
                5309898
                28186104
                4d867078-ca10-4156-a826-e8e3e111f140
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 14 May 2016
                : 20 December 2016
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