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      High Connectivity in the Deepwater Snapper Pristipomoides filamentosus (Lutjanidae) across the Indo-Pacific with Isolation of the Hawaiian Archipelago

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          Abstract

          In the tropical Indo-Pacific, most phylogeographic studies have focused on the shallow-water taxa that inhabit reefs to approximately 30 m depth. Little is known about the large predatory fishes, primarily snappers (subfamily Etelinae) and groupers (subfamily Epinephelinae) that occur at 100–400 m. These long-lived, slow-growing species support fisheries across the Indo-Pacific, yet no comprehensive genetic surveys within this group have been conducted. Here we contribute the first range-wide survey of a deepwater Indo-Pacific snapper, Pristipomoides filamentosus, with special focus on Hawai'i. We applied mtDNA cytochrome b and 11 microsatellite loci to 26 samples ( N = 1,222) collected across 17,000 km from Hawai'i to the western Indian Ocean. Results indicate that P. filamentosus is a highly dispersive species with low but significant population structure (mtDNA Φ ST = 0.029, microsatellite F ST = 0.029) due entirely to the isolation of Hawai'i. No population structure was detected across 14,000 km of the Indo-Pacific from Tonga in the Central Pacific to the Seychelles in the western Indian Ocean, a pattern rarely observed in reef species. Despite a long pelagic phase (60–180 days), interisland dispersal as adults, and extensive gene flow across the Indo-Pacific, P. filamentosus is unable to maintain population connectivity with Hawai'i. Coalescent analyses indicate that P. filamentosus may have colonized Hawai'i 26 K–52 K y ago against prevailing currents, with dispersal away from Hawai'i dominating migration estimates. P. filamentosus harbors low genetic diversity in Hawai'i, a common pattern in marine fishes, and our data indicate a single archipelago-wide stock. However, like the Hawaiian Grouper, Hyporthodus quernus, this snapper had several significant pairwise comparisons ( F ST) clustered around the middle of the archipelago (St. Rogatien, Brooks Banks, Gardner) indicating that this region may be isolated or (more likely) receives input from Johnston Atoll to the south.

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          Estimation of average heterozygosity and genetic distance from a small number of individuals.

          M Nei (1978)
          The magnitudes of the systematic biases involved in sample heterozygosity and sample genetic distances are evaluated, and formulae for obtaining unbiased estimates of average heterozygosity and genetic distance are developed. It is also shown that the number of individuals to be used for estimating average heterozygosity can be very small if a large number of loci are studied and the average heterozygosity is low. The number of individuals to be used for estimating genetic distance can also be very small if the genetic distance is large and the average heterozygosity of the two species compared is low.
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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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              Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution.

              A mismatch distribution is a tabulation of the number of pairwise differences among all DNA sequences in a sample. In a population that has been stationary for a long time these distributions from nonrecombinant DNA sequences become ragged and erratic, whereas a population that has been growing generates mismatch distributions that are smooth and have a peak. The position of the peak reflects the time of the population growth. The signature of an ancient population expansion is apparent even in the low-resolution mtDNA typings described by Merriwether et al. (1991). The smoothness of the mismatch distribution, an indicator of population expansion, is hardly affected by population structure, whereas mean sequence divergence increases in a pooled sample from highly isolated subpopulations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                22 December 2011
                : 6
                : 12
                : e28913
                Affiliations
                [1 ]Hawai'i Institute of Marine Biology, University of Hawai'i at Mānoa, Kane'ohe, Hawai'i, United States of America
                [2 ]Human Performance Laboratory, Humboldt State University, Arcata, California, United States of America
                [3 ]Hawai'i Undersea Research Laboratory, University of Hawai'i at Mānoa, Honolulu, Hawai'i, United States of America
                [4 ]Western Australian Fisheries and Marine Research Laboratories, Department of Fisheries, North Beach, Australia
                [5 ]Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, California, United States of America
                Smithsonian Institution National Zoological Park, United States of America
                Author notes

                Conceived and designed the experiments: MRG CK SJN BWB. Performed the experiments: MRG SAJ LS. Analyzed the data: MRG SAJ LS BWB. Contributed reagents/materials/analysis tools: MRG CK SJN BWB. Wrote the paper: MRG BWB.

                Article
                PONE-D-11-16935
                10.1371/journal.pone.0028913
                3245230
                22216141
                00f77e98-900e-4304-83cc-3c925baf61eb
                Gaither et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 31 August 2011
                : 17 November 2011
                Page count
                Pages: 13
                Categories
                Research Article
                Biology
                Computational Biology
                Population Genetics
                Gene Flow
                Haplotypes
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Population Genetics
                Gene Flow
                Haplotypes
                Genetics
                Heredity
                Gene Flow
                Population Genetics
                Gene Flow
                Haplotypes
                Marine Biology
                Fisheries Science
                Population Biology
                Population Genetics
                Gene Flow
                Haplotypes
                Zoology
                Animal Phylogenetics
                Ichthyology

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                Uncategorized

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