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      Genetic connectivity of lionfish ( Pterois volitans) in marine protected areas of the Gulf of Mexico and Caribbean Sea

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          Abstract

          Lionfish ( Pterois volitans) have rapidly invaded the tropical Atlantic and spread across the wider Caribbean in a relatively short period of time. Because of its high invasion capacity, we used it as a model to identify the connectivity among nine marine protected areas (MPAs) situated in four countries in the Gulf of Mexico and the Caribbean Sea. This study provides evidence of local genetic differentiation of P. volitans in the Gulf of Mexico and the Caribbean Sea. A total of 475 lionfish samples were characterized with 12 microsatellites, with 6–20 alleles per locus. Departures from Hardy–Weinberg equilibrium (HWE) were found in 10 of the 12 loci, all caused by heterozygous excess. Moderate genetic differentiation was observed between Chiriviche, Venezuela and Xcalak, México localities ( F ST = 0.012), and between the Los Roques and the Veracruz ( F ST = 0.074) sites. STRUCTURE analysis found that four genetic entities best fit our data. A unique genetic group in the Gulf of Mexico may imply that the lionfish invasion unfolded both in a counterclockwise manner in the Gulf of Mexico. In spite of the notable dispersion of P. volitans, our results show some genetic structure, as do other noninvasive Caribbean fish species, suggesting that the connectivity in some MPAs analyzed in the Caribbean is limited and caused by only a few source individuals with subsequent genetic drift leading to local genetic differentiation. This indicates that P. volitans dispersion could be caused by mesoscale phenomena, which produce stochastic connectivity pulses. Due to the isolation of some MPAs from others, these findings may hold a promise for local short‐term control of by means of intensive fishing, even in MPAs, and may have regional long‐term effects.

          Abstract

          Our findings demonstrate that there is genetic differentiation at local and regional scales.We suggest that the colonization of each geographic area has been temporary pulses, probably caused by mesoscale phenomena, and intensified with the presence of self‐recruitment. The genetic diversity of Pterois volitans in the Gulf and the Caribbean showed that the number of organisms that originated the invasion was much higher than the one mentioned in the literature.

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          Most cited references39

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          What can genetics tell us about population connectivity?

          Genetic data are often used to assess 'population connectivity' because it is difficult to measure dispersal directly at large spatial scales. Genetic connectivity, however, depends primarily on the absolute number of dispersers among populations, whereas demographic connectivity depends on the relative contributions to population growth rates of dispersal vs. local recruitment (i.e. survival and reproduction of residents). Although many questions are best answered with data on genetic connectivity, genetic data alone provide little information on demographic connectivity. The importance of demographic connectivity is clear when the elimination of immigration results in a shift from stable or positive population growth to negative population growth. Otherwise, the amount of dispersal required for demographic connectivity depends on the context (e.g. conservation or harvest management), and even high dispersal rates may not indicate demographic interdependence. Therefore, it is risky to infer the importance of demographic connectivity without information on local demographic rates and how those rates vary over time. Genetic methods can provide insight on demographic connectivity when combined with these local demographic rates, data on movement behaviour, or estimates of reproductive success of immigrants and residents. We also consider the strengths and limitations of genetic measures of connectivity and discuss three concepts of genetic connectivity that depend upon the evolutionary criteria of interest: inbreeding connectivity, drift connectivity, and adaptive connectivity. To conclude, we describe alternative approaches for assessing population connectivity, highlighting the value of combining genetic data with capture-mark-recapture methods or other direct measures of movement to elucidate the complex role of dispersal in natural populations.
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            Using the AMOVA framework to estimate a standardized genetic differentiation measure.

            Comparison of population structure between studies can be difficult, because the value of the often-used FST-statistic depends on the amount of genetic variation within populations. Recently, a standardized measure of genetic differentiation was developed based on GST, which addressed this problem, though no method was provided to estimate this standardized measure without bias. Here I present a method to estimate a standardized measure of population differentiation based on the analysis of molecular variance framework. One advantage of the method is that it can be readily expanded to include different hierarchical levels in the tested population structure.
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              Larval dispersal connects fish populations in a network of marine protected areas.

              Networks of no-take marine protected areas (MPAs) have been widely advocated for the conservation of marine biodiversity. But for MPA networks to be successful in protecting marine populations, individual MPAs must be self-sustaining or adequately connected to other MPAs via dispersal. For marine species with a dispersive larval stage, populations within MPAs require either the return of settlement-stage larvae to their natal reserve or connectivity among reserves at the spatial scales at which MPA networks are implemented. To date, larvae have not been tracked when dispersing from one MPA to another, and the relative magnitude of local retention and connectivity among MPAs remains unknown. Here we use DNA parentage analysis to provide the first direct estimates of connectivity of a marine fish, the orange clownfish (Amphiprion percula), in a proposed network of marine reserves in Kimbe Bay, Papua New Guinea. Approximately 40% of A. percula larvae settling into anemones in an island MPA at 2 different times were derived from parents resident in the reserve. We also located juveniles spawned by Kimbe Island residents that had dispersed as far as 35 km to other proposed MPAs, the longest distance that marine larvae have been directly tracked. These dispersers accounted for up to 10% of the recruitment in the adjacent MPAs. Our findings suggest that MPA networks can function to sustain resident populations both by local replenishment and through larval dispersal from other reserves. More generally, DNA parentage analysis provides a direct method for measuring larval dispersal for other marine organisms.
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                Author and article information

                Contributors
                earias@cinvestav.mx
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                16 April 2020
                May 2020
                : 10
                : 9 ( doiID: 10.1002/ece3.v10.9 )
                : 3844-3855
                Affiliations
                [ 1 ] Laboratorio de Ecología de Ecosistemas de Arrecifes Coralinos Departamento de Recursos del Mar Centro de Investigación y de Estudios Avanzados del I.P.N.‐ Unidad Mérida Mérida México
                [ 2 ] Department of Biological Sciences Marquette University Milwaukee WI USA
                [ 3 ] Unidad de Bioquímica Molecular de Plantas Centro de Investigación Científica de Yucatán Mérida México
                [ 4 ] PSL Research University: EPHE‐UPVD‐CNRS USR 3278 CRIOBE Université de Perpignan Perpignan Cedex France
                [ 5 ] Laboratoire d'Excellence « CORAIL » Perpignan Cedex France
                [ 6 ] Departamento de Estudios Ambientales Universidad Simón Bolívar Caracas Venezuela
                [ 7 ] Laboratorio de Arrecifes Coralinos. Carrera de Biología Universidad Veracruzana Tuxpan México
                [ 8 ] Instituto de Ciencias Marinas y Pesquerías Universidad Veracruzana Boca del Río México
                [ 9 ] Healthy Reefs for Healthy People Initiative Ciudad de Guatemala Guatemala
                [ 10 ] Bay Islands Association Utila Honduras Utila Honduras
                [ 11 ] Comisión Nacional de Áreas Naturales Protegidas Parque Nacional Arrecifes de Puerto Morelos Puerto Morelos México
                Author notes
                [*] [* ] Correspondence

                Jesus E. Arias‐González, Laboratorio de Ecología de Ecosistemas de Arrecifes Coralinos, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del I.P.N.‐ Unidad Mérida, Ant. Carr. a Progreso km 6, A.P. 73, Cordemex, 97310 Mérida, Yucatán, México.

                Email: earias@ 123456cinvestav.mx

                Author information
                https://orcid.org/0000-0001-5217-2689
                https://orcid.org/0000-0003-1368-9639
                http://orcid.org/0000-0002-5689-5371
                https://orcid.org/0000-0002-4110-790X
                https://orcid.org/0000-0001-8880-9338
                https://orcid.org/0000-0001-7815-4120
                https://orcid.org/0000-0003-4155-9719
                https://orcid.org/0000-0003-4888-4688
                https://orcid.org/0000-0002-1968-2692
                https://orcid.org/0000-0002-9563-2064
                Article
                ECE35829
                10.1002/ece3.5829
                7244795
                eac761f7-7718-47f0-a4e5-15196c2ed2e2
                © 2019 The Authors. Ecology and Evolution 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
                : 08 April 2019
                : 01 October 2019
                : 03 October 2019
                Page count
                Figures: 4, Tables: 5, Pages: 12, Words: 9276
                Funding
                Funded by: Consejo Nacional de Ciencia y Tecnología (CONACyT) , open-funder-registry 10.13039/501100003141;
                Award ID: 215434
                Award ID: 2018-000022-01EXTV-00437
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                May 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.2 mode:remove_FC converted:23.05.2020

                Evolutionary Biology
                caribbean sea,founder event,genetic structure,invasive species,lionfish,marine protected areas,microsatellites

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