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      Demographic Processes Underlying Subtle Patterns of Population Structure in the Scalloped Hammerhead Shark, Sphyrna lewini

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          Abstract

          Genetic diversity (θ), effective population size (N e), and contemporary levels of gene flow are important parameters to estimate for species of conservation concern, such as the globally endangered scalloped hammerhead shark, Sphyrna lewini. Therefore, we have reconstructed the demographic history of S. lewini across its Eastern Pacific (EP) range by applying classical and coalescent population genetic methods to a combination of 15 microsatellite loci and mtDNA control region sequences. In addition to significant population genetic structure and isolation-by-distance among seven coastal sites between central Mexico and Ecuador, the analyses revealed that all populations have experienced a bottleneck and that all current values of θ are at least an order of magnitude smaller than ancestral θ, indicating large decreases in N e (θ = 4N eμ), where μ is the mutation rate. Application of the isolation-with-migration (IM) model showed modest but significant genetic connectivity between most sampled sites (point estimates of Nm = 0.1–16.7), with divergence times (t) among all populations significantly greater than zero. Using a conservative (i.e., slow) fossil-based taxon-specific phylogenetic calibration for mtDNA mutation rates, posterior probability distributions (PPDs) for the onset of the decline in N e predate modern fishing in this region. The cause of decline over the last several thousand years is unknown but is highly atypical as a post-glacial demographic history. Regardless of the cause, our data and analyses suggest that S. lewini was far more abundant throughout the EP in the past than at present.

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          Detection of reduction in population size using data from microsatellite loci.

          We demonstrate that the mean ratio of the number of alleles to the range in allele size, which we term M, calculated from a population sample of microsatellite loci, can be used to detect reductions in population size. Using simulations, we show that, for a general class of mutation models, the value of M decreases when a population is reduced in size. The magnitude of the decrease is positively correlated with the severity and duration of the reduction in size. We also find that the rate of recovery of M following a reduction in size is positively correlated with post-reduction population size, but that recovery occurs in both small and large populations. This indicates that M can distinguish between populations that have been recently reduced in size and those which have been small for a long time. We employ M to develop a statistical test for recent reductions in population size that can detect such changes for more than 100 generations with the post-reduction demographic scenarios we examine. We also compute M for a variety of populations and species using microsatellite data collected from the literature. We find that the value of M consistently predicts the reported demographic history for these populations. This method, and others like it, promises to be an important tool for the conservation and management of populations that are in need of intervention or recovery.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                14 July 2011
                : 6
                : 7
                : e21459
                Affiliations
                [1 ]Department of Biological Sciences, Clemson University, Clemson, South Carolina, United States of America
                [2 ]Department of Wildlife, Fish, and Conservation Biology, University of California Davis, Davis, California, United States of America
                [3 ]Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), La Paz, Mexico
                [4 ]Escuela de Pesca del Pacífico Oriental (EPESPO), Manta, Ecuador
                University of Canterbury, New Zealand
                Author notes

                Conceived and designed the experiments: HAN PK FG-M JM-O PBM. Performed the experiments: HAN PBM. Analyzed the data: HAN PBM. Contributed reagents/materials/analysis tools: HAN PK FG-M JM-O PBM. Wrote the paper: HAN PBM. Critically edited and revised previous drafts of the manuscript: APK FGM JMO. Helped with collection of samples and organization of field work: APK FGM JMO.

                Article
                PONE-D-11-01874
                10.1371/journal.pone.0021459
                3137562
                21789171
                9547589f-8635-461c-8590-a4ea42361d7c
                Nance 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
                : 24 January 2011
                : 2 June 2011
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Computational Biology
                Population Genetics
                Effective Population Size
                Gene Flow
                Genetic Drift
                Evolutionary Biology
                Evolutionary Processes
                Genetic Drift
                Evolutionary Ecology
                Evolutionary Genetics
                Population Genetics
                Genetics
                Population Genetics
                Marine Biology
                Fisheries Science
                Marine Conservation
                Population Biology
                Population Genetics
                Zoology
                Ichthyology

                Uncategorized
                Uncategorized

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