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      Large‐scale genetic panmixia in the blue shark ( Prionace glauca): A single worldwide population, or a genetic lag‐time effect of the “grey zone” of differentiation?

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          Abstract

          The blue shark Prionace glauca, among the most common and widely studied pelagic sharks, is a top predator, exhibiting the widest distribution range. However, little is known about its population structure and spatial dynamics. With an estimated removal of 10–20 million individuals per year by fisheries, the species is classified as “Near Threatened” by International Union for Conservation of Nature. We lack the knowledge to forecast the long‐term consequences of such a huge removal on this top predator itself and on its trophic network. The genetic analysis of more than 200 samples collected at broad scale (from Mediterranean Sea, North Atlantic and Pacific Oceans) using mt DNA and nine microsatellite markers allowed to detect signatures of genetic bottlenecks but a nearly complete genetic homogeneity across the entire studied range. This apparent panmixia could be explained by a genetic lag‐time effect illustrated by simulations of demographic changes that were not detectable through standard genetic analysis before a long transitional phase here introduced as the “population grey zone.” The results presented here can thus encompass distinct explanatory scenarios spanning from a single demographic population to several independent populations. This limitation prevents the genetic‐based delineation of stocks and thus the ability to anticipate the consequences of severe depletions at all scales. More information is required for the conservation of population(s) and management of stocks, which may be provided by large‐scale sampling not only of individuals worldwide, but also of loci genomewide.

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          Most cited references83

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          Cascading effects of the loss of apex predatory sharks from a coastal ocean.

          Impacts of chronic overfishing are evident in population depletions worldwide, yet indirect ecosystem effects induced by predator removal from oceanic food webs remain unpredictable. As abundances of all 11 great sharks that consume other elasmobranchs (rays, skates, and small sharks) fell over the past 35 years, 12 of 14 of these prey species increased in coastal northwest Atlantic ecosystems. Effects of this community restructuring have cascaded downward from the cownose ray, whose enhanced predation on its bay scallop prey was sufficient to terminate a century-long scallop fishery. Analogous top-down effects may be a predictable consequence of eliminating entire functional groups of predators.
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            What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity.

            We review commonly used population definitions under both the ecological paradigm (which emphasizes demographic cohesion) and the evolutionary paradigm (which emphasizes reproductive cohesion) and find that none are truly operational. We suggest several quantitative criteria that might be used to determine when groups of individuals are different enough to be considered 'populations'. Units for these criteria are migration rate (m) for the ecological paradigm and migrants per generation (Nm) for the evolutionary paradigm. These criteria are then evaluated by applying analytical methods to simulated genetic data for a finite island model. Under the standard parameter set that includes L = 20 High mutation (microsatellite-like) loci and samples of S = 50 individuals from each of n = 4 subpopulations, power to detect departures from panmixia was very high ( approximately 100%; P < 0.001) even with high gene flow (Nm = 25). A new method, comparing the number of correct population assignments with the random expectation, performed as well as a multilocus contingency test and warrants further consideration. Use of Low mutation (allozyme-like) markers reduced power more than did halving S or L. Under the standard parameter set, power to detect restricted gene flow below a certain level X (H(0): Nm < X) can also be high, provided that true Nm < or = 0.5X. Developing the appropriate test criterion, however, requires assumptions about several key parameters that are difficult to estimate in most natural populations. Methods that cluster individuals without using a priori sampling information detected the true number of populations only under conditions of moderate or low gene flow (Nm < or = 5), and power dropped sharply with smaller samples of loci and individuals. A simple algorithm based on a multilocus contingency test of allele frequencies in pairs of samples has high power to detect the true number of populations even with Nm = 25 but requires more rigorous statistical evaluation. The ecological paradigm remains challenging for evaluations using genetic markers, because the transition from demographic dependence to independence occurs in a region of high migration where genetic methods have relatively little power. Some recent theoretical developments and continued advances in computational power provide hope that this situation may change in the future.
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              Collapse and conservation of shark populations in the Northwest Atlantic.

              Overexploitation threatens the future of many large vertebrates. In the ocean, tunas and sea turtles are current conservation concerns because of this intense pressure. The status of most shark species, in contrast, remains uncertain. Using the largest data set in the Northwest Atlantic, we show rapid large declines in large coastal and oceanic shark populations. Scalloped hammerhead, white, and thresher sharks are each estimated to have declined by over 75% in the past 15 years. Closed-area models highlight priority areas for shark conservation, and the need to consider effort reallocation and site selection if marine reserves are to benefit multiple threatened species.
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                Author and article information

                Contributors
                sophie.arnaud@ifremer.fr
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                22 February 2018
                June 2018
                : 11
                : 5 ( doiID: 10.1111/eva.2018.11.issue-5 )
                : 614-630
                Affiliations
                [ 1 ] IFREMER, UMR MARBEC, Station de Sète Sète France
                [ 2 ] OREME – Station Marine Université Montpellier Sète France
                [ 3 ] CNRS, Institut des Sciences de l'Evolution Université Montpellier Montpellier France
                Author notes
                [*] [* ] Correspondence

                Sophie Arnaud‐Haond, IFREMER, UMR MARBEC, Station de Sète, Sète, France.

                Email: sophie.arnaud@ 123456ifremer.fr

                [†]

                These authors equally contributed to the article.

                Author information
                http://orcid.org/0000-0001-6369-5426
                Article
                EVA12591
                10.1111/eva.12591
                5978958
                29875806
                227485d4-4859-4bbe-b9b6-99b93ce0cac5
                © 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 04 September 2017
                : 12 December 2017
                Page count
                Figures: 7, Tables: 4, Pages: 17, Words: 13207
                Funding
                Funded by: FFP (“France Filière Pêche”)
                Funded by: Conseil Régional Languedoc‐Roussillon
                Funded by: Conseil Départemental de l'Hérault
                Funded by: Conseil Départemental des Pyrénées‐Orientales
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                eva12591
                June 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.0 mode:remove_FC converted:31.05.2018

                Evolutionary Biology
                blue shark,conservation,fisheries,genetic panmixia,prionace glauca,stock
                Evolutionary Biology
                blue shark, conservation, fisheries, genetic panmixia, prionace glauca, stock

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