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      A genome-wide assessment of stages of elevational parapatry in Bornean passerine birds reveals no introgression: implications for processes and patterns of speciation

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          Abstract

          Topographically complex regions often contain the close juxtaposition of closely related species along elevational gradients. The evolutionary causes of these elevational replacements, and thus the origin and maintenance of a large portion of species diversity along elevational gradients, are usually unclear because ecological differentiation along a gradient or secondary contact following allopatric diversification can produce the same pattern. We used reduced representation genomic sequencing to assess genetic relationships and gene flow between three parapatric pairs of closely related songbird taxa ( Arachnothera spiderhunters, Chloropsis leafbirds, and Enicurus forktails) along an elevational gradient in Borneo. Each taxon pair presents a different elevational range distribution across the island, yet results were uniform: little or no gene flow was detected in any pairwise comparisons. These results are congruent with an allopatric “species-pump” model for generation of species diversity and elevational parapatry of congeners on Borneo, rather than in situ generation of species by “ecological speciation” along an elevational gradient.

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          Most cited references46

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          Speciation in amazonian forest birds.

          J Haffer (1969)
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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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              Niche filling slows the diversification of Himalayan songbirds.

              Speciation generally involves a three-step process--range expansion, range fragmentation and the development of reproductive isolation between spatially separated populations. Speciation relies on cycling through these three steps and each may limit the rate at which new species form. We estimate phylogenetic relationships among all Himalayan songbirds to ask whether the development of reproductive isolation and ecological competition, both factors that limit range expansions, set an ultimate limit on speciation. Based on a phylogeny for all 358 species distributed along the eastern elevational gradient, here we show that body size and shape differences evolved early in the radiation, with the elevational band occupied by a species evolving later. These results are consistent with competition for niche space limiting species accumulation. Even the elevation dimension seems to be approaching ecological saturation, because the closest relatives both inside the assemblage and elsewhere in the Himalayas are on average separated by more than five million years, which is longer than it generally takes for reproductive isolation to be completed; also, elevational distributions are well explained by resource availability, notably the abundance of arthropods, and not by differences in diversification rates in different elevational zones. Our results imply that speciation rate is ultimately set by niche filling (that is, ecological competition for resources), rather than by the rate of acquisition of reproductive isolation.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                18 May 2017
                2017
                : 5
                : e3335
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology and Biodiversity Institute, The University of Kansas , Lawrence, KS, USA
                [2 ]Department of Biology, University of Florida , Gainesville, FL, USA
                [3 ]Faculty of Natural Science and Sustainability, University College Sabah Foundation , Kota Kinabalu, Sabah, Malaysia
                [4 ]Sabah Parks , Kota Kinabalu, Sabah, Malaysia
                [5 ]Museum of Natural Science and Department of Biological Sciences, Louisiana State University , Baton Rouge, LA, USA
                Author information
                http://orcid.org/0000-0001-6513-2344
                Article
                3335
                10.7717/peerj.3335
                5438588
                28533979
                17e51be9-a80a-4ac0-bb17-4865cac6a685
                © 2017 Moyle et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 15 June 2016
                : 19 April 2017
                Funding
                Funded by: National Science Foundation
                Award ID: DEB-02288688, DEB-1241181, and DEB-1241059
                Funded by: Coypu Foundation of Louisiana
                Funded by: National Geographic Society
                Funded by: Louisiana State University
                Funded by: The University of Kansas
                Funded by: KU Genome Sequencing Core
                Award ID: 5P20GM103638
                Funded by: KU Advanced Computing Facility
                Award ID: CNS 1337899
                This work was supported by grants from the National Science Foundation (DEB-02288688, DEB-1241181, and DEB-1241059), Coypu Foundation of Louisiana, National Geographic Society, Louisiana State University, and The University of Kansas. The KU Genome Sequencing Core (supported by NIH grant 5P20GM103638 to E.A. Lundquist) and the KU Advanced Computing Facility (partially funded by NSF grant CNS 1337899 to A.T. Peterson) granted use of their facilities. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Biodiversity
                Biogeography
                Zoology

                parapatry,speciation,species pump,elevation,borneo,elevational cline

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