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      Non-equilibrium estimates of gene flow inferred from nuclear genealogies suggest that Iberian and North African wall lizards ( Podarcis spp.) are an assemblage of incipient species

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      1 , 2 , , 1 , 3 , 1 , 3
      BMC Evolutionary Biology
      BioMed Central

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          Abstract

          Background

          The study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them. Iberian and North African wall lizards ( Podarcis) constitute a cryptic species complex for which previous assessments of mitochondrial DNA (mtDNA) and allozyme variation are concordant in describing the existence of several highly differentiated evolutionary units. However, these studies report important differences suggesting the occurrence of gene flow among forms. Here we study sequence variation in two nuclear introns, β-fibint7 and 6-Pgdint7, to further investigate overall evolutionary dynamics and test hypotheses related to species delimitation within this complex.

          Results

          Both nuclear gene genealogies fail to define species as monophyletic. To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both F ST -based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow. Equilibrium estimates of gene flow suggest widespread introgression between species, but coalescent estimates describe virtually zero admixture between most (but not all) species pairs. This suggests that although gene flow among forms may have occurred the main cause for species polyphyly is incomplete lineage sorting, implying that most forms have been isolated since their divergence. This observation is therefore in accordance with previous reports of strong differentiation based on mtDNA and allozyme data.

          Conclusion

          These results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries. Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

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          Most cited references60

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          Molecular Cloning : A Laboratory Manual

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            Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.

            A new statistical method for estimating divergence dates of species from DNA sequence data by a molecular clock approach is developed. This method takes into account effectively the information contained in a set of DNA sequence data. The molecular clock of mitochondrial DNA (mtDNA) was calibrated by setting the date of divergence between primates and ungulates at the Cretaceous-Tertiary boundary (65 million years ago), when the extinction of dinosaurs occurred. A generalized least-squares method was applied in fitting a model to mtDNA sequence data, and the clock gave dates of 92.3 +/- 11.7, 13.3 +/- 1.5, 10.9 +/- 1.2, 3.7 +/- 0.6, and 2.7 +/- 0.6 million years ago (where the second of each pair of numbers is the standard deviation) for the separation of mouse, gibbon, orangutan, gorilla, and chimpanzee, respectively, from the line leading to humans. Although there is some uncertainty in the clock, this dating may pose a problem for the widely believed hypothesis that the pipedal creature Australopithecus afarensis, which lived some 3.7 million years ago at Laetoli in Tanzania and at Hadar in Ethiopia, was ancestral to man and evolved after the human-ape splitting. Another likelier possibility is that mtDNA was transferred through hybridization between a proto-human and a proto-chimpanzee after the former had developed bipedalism.
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              Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach.

              A maximum likelihood estimator based on the coalescent for unequal migration rates and different subpopulation sizes is developed. The method uses a Markov chain Monte Carlo approach to investigate possible genealogies with branch lengths and with migration events. Properties of the new method are shown by using simulated data from a four-population n-island model and a source-sink population model. Our estimation method as coded in migrate is tested against genetree; both programs deliver a very similar likelihood surface. The algorithm converges to the estimates fairly quickly, even when the Markov chain is started from unfavorable parameters. The method was used to estimate gene flow in the Nile valley by using mtDNA data from three human populations.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2008
                26 February 2008
                : 8
                : 63
                Affiliations
                [1 ]CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos. Campus Agrário de Vairão, 4485-661 Vairão, Portugal
                [2 ]Department of Genetics, Rutgers, the State University of New Jersey. Piscataway, NJ 08854, USA
                [3 ]Departmento de Zoologia e Antropologia, Faculdade de Ciências da Universidade do Porto, Praça Gomes Teixeira, 4099-002 Porto, Portugal
                Article
                1471-2148-8-63
                10.1186/1471-2148-8-63
                2277379
                18302778
                a7ca55af-bde4-4c53-8f46-f01c860175ad
                Copyright © 2008 Pinho et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 8 October 2007
                : 26 February 2008
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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