{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,8]],"date-time":"2026-05-08T15:32:37Z","timestamp":1778254357079,"version":"3.51.4"},"reference-count":74,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,5,26]],"date-time":"2020-05-26T00:00:00Z","timestamp":1590451200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,5,26]],"date-time":"2020-05-26T00:00:00Z","timestamp":1590451200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Severe disturbances can substantially alter eco-evolutionary processes and dynamics. While the impacts of catastrophic events on the biophysical attributes of communities are sometimes assessed, their effects on the genetic patterns of species remain poorly understood. To characterize how severe disturbances impact species at the molecular level, we examined the effects of the most energetic North Atlantic hurricane season in 50 years on the genetic diversity and structure of a dispersal-limited isopod, <jats:italic>Gnathia marleyi<\/jats:italic>. We sequenced a portion of the cytochrome oxidase I gene for 432 gnathiids, collected from six localities, ranging from western Puerto Rico to St John, US Virgin Islands. Importantly, multiple years of pre-hurricane sample collection allowed us to characterize temporal genetic patterns under undisturbed conditions and detect the changes subsequent to the 2017 hurricanes. Our results revealed no change to genetic diversity or structure for the years prior to the 2017 hurricanes, with genetic structure occurring at the local and regional levels, with three main clusters corresponding to Southwest Puerto Rico, East Puerto Rico, and the US Virgin Islands. However, directly following the 2017 hurricanes, genetic diversity increased at five of the six sampled localities. Additionally, we found a clear homogenizing effect prompted by increased shared genetic diversity among geographically distant regions and sites that resulted in substantially decreased among-region and among-site differentiation. Our work shows that severe disturbances caused by major tropical hurricanes facilitate gene-flow and increase overall genetic diversity and population admixture of dispersal limited coral reef species, potentially impacting the ecology and evolution of a key regional endemic.<\/jats:p>","DOI":"10.1038\/s41598-020-64779-7","type":"journal-article","created":{"date-parts":[[2020,5,26]],"date-time":"2020-05-26T10:02:38Z","timestamp":1590487358000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Hurricane-induced disturbance increases genetic diversity and population admixture of the direct-brooding isopod, Gnathia marleyi"],"prefix":"10.1038","volume":"10","author":[{"given":"J. Andr\u00e9s","family":"Pag\u00e1n","sequence":"first","affiliation":[]},{"given":"Ana","family":"Ver\u00edssimo","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2652-7498","authenticated-orcid":false,"given":"Paul C.","family":"Sikkel","sequence":"additional","affiliation":[]},{"given":"Raquel","family":"Xavier","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2020,5,26]]},"reference":[{"key":"64779_CR1","doi-asserted-by":"crossref","unstructured":"White, P. S. & Jentsch, A. The Search for Generality in Studies of Disturbance and Ecosystem Dynamics. in Progress in Botany (eds. Esser, K., L\u00fcttge, U., Kadereit, J. W. & Beyschlag, W.) vol. 62 399\u2013450 (Springer Berlin Heidelberg, 2001).","DOI":"10.1007\/978-3-642-56849-7_17"},{"key":"64779_CR2","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/BF00304732","volume":"2","author":"WJ Walsh","year":"1983","unstructured":"Walsh, W. J. Stability of a coral reef fish community following a catastrophic storm. Coral Reefs 2, 49\u201363 (1983).","journal-title":"Coral Reefs"},{"key":"64779_CR3","doi-asserted-by":"publisher","first-page":"1185","DOI":"10.2307\/1938326","volume":"65","author":"LA Levin","year":"1984","unstructured":"Levin, L. A. Life history and dispersal patterns in a dense infaunal polychaete assemblage: community structure and response to disturbance. Ecology 65, 1185\u20131200 (1984).","journal-title":"Ecology"},{"key":"64779_CR4","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1093\/ee\/15.4.850","volume":"15","author":"RN Coulson","year":"1986","unstructured":"Coulson, R. N. et al. Response of the southern pine bark beetle guild (Coleoptera: Scolytidae) to host disturbance. Environ. Entomol. 15, 850\u2013858 (1986).","journal-title":"Environ. Entomol."},{"key":"64779_CR5","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1146\/annurev.es.15.110184.002033","volume":"15","author":"WP Sousa","year":"1984","unstructured":"Sousa, W. P. The role of disturbance in natural communities. Annu. Rev. Ecol. Syst. 15, 353\u2013391 (1984).","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"64779_CR6","doi-asserted-by":"publisher","first-page":"758","DOI":"10.2307\/1313098","volume":"47","author":"MG Turner","year":"1997","unstructured":"Turner, M. G., Dale, V. H. & Everham, E. H. Fires, hurricanes, and volcanoes: comparing large disturbances. BioScience 47, 758\u2013768 (1997).","journal-title":"BioScience"},{"key":"64779_CR7","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1016\/j.tree.2013.08.005","volume":"28","author":"SC Banks","year":"2013","unstructured":"Banks, S. C. et al. How does ecological disturbance influence genetic diversity? Trends Ecol. Evol. 28, 670\u2013679 (2013).","journal-title":"Trends Ecol. Evol."},{"key":"64779_CR8","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.1420-9101.2005.00976.x","volume":"19","author":"M Alleaume-Benharira","year":"2006","unstructured":"Alleaume-Benharira, M., Pen, I. R. & Ronce, O. Geographical patterns of adaptation within a species\u2019 range: interactions between drift and gene flow. J. Evol. Biol. 19, 203\u2013215 (2006).","journal-title":"J. Evol. Biol."},{"key":"64779_CR9","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1111\/j.1365-2435.2006.01228.x","volume":"21","author":"D Garant","year":"2007","unstructured":"Garant, D., Forde, S. E. & Hendry, A. P. The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct. Ecol. 21, 434\u2013443 (2007).","journal-title":"Funct. Ecol."},{"key":"64779_CR10","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1126\/science.1087486","volume":"302","author":"LB Beheregaray","year":"2003","unstructured":"Beheregaray, L. B. Genes record a prehistoric colcano eruption in the Galapagos. Science 302, 75\u201375 (2003).","journal-title":"Science"},{"key":"64779_CR11","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1111\/j.1600-0706.2010.18765.x","volume":"120","author":"SC Banks","year":"2011","unstructured":"Banks, S. C. et al. Starting points for small mammal population recovery after wildfire: recolonisation or residual populations? Oikos 120, 26\u201337 (2011).","journal-title":"Oikos"},{"key":"64779_CR12","doi-asserted-by":"publisher","first-page":"856","DOI":"10.1890\/11-0627.1","volume":"22","author":"SF Spear","year":"2012","unstructured":"Spear, S. F., Crisafulli, C. M. & Storfer, A. Genetic structure among coastal tailed frog populations at Mount St. Helens is moderated by post-disturbance management. Ecol. Appl. 22, 856\u2013869 (2012).","journal-title":"Ecol. Appl."},{"key":"64779_CR13","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-41729-6","volume":"9","author":"D Ferreira","year":"2019","unstructured":"Ferreira, D., Pinho, C., Brito, J. C. & Santos, X. Increase of genetic diversity indicates ecological opportunities in recurrent-fire landscapes for wall lizards. Sci. Rep. 9, 5383 (2019).","journal-title":"Sci. Rep."},{"key":"64779_CR14","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1002\/9781118525258.ch13","volume-title":"Landscape Genetics","author":"Kimberly A. Selkoe","year":"2015","unstructured":"Selkoe, K. A., Scribner, K. T. & Galindo, H. M. Waterscape Genetics - Applications of Landscape Genetics to Rivers, Lakes, and Seas. in Landscape Genetics (eds. Balkenhol, N., Cushman, S. A., Storfer, A. T. & Waits, L. P.) 220\u2013246 (John Wiley & Sons, Ltd, 2015). https:\/\/doi.org\/10.1002\/9781118525258.ch13."},{"key":"64779_CR15","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1890\/04-0141","volume":"86","author":"TA Gardner","year":"2005","unstructured":"Gardner, T. A., C\u00f4t\u00e9, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86, 174\u2013184 (2005).","journal-title":"Ecology"},{"key":"64779_CR16","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1007\/BF02798646","volume":"29","author":"H Greening","year":"2006","unstructured":"Greening, H., Doering, P. & Corbett, C. Hurricane impacts on coastal ecosystems. Estuaries Coasts 29, 877\u2013879 (2006).","journal-title":"Estuaries Coasts"},{"key":"64779_CR17","first-page":"749","volume":"214","author":"JD Woodley","year":"1981","unstructured":"Woodley, J. D. et al. Hurricane Allen\u2019s impact on Jamaican coral reefs. Sci. New Ser. 214, 749\u2013755 (1981).","journal-title":"Sci. New Ser."},{"key":"64779_CR18","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/BF00270353","volume":"5","author":"ML Harmelin-Vivien","year":"1986","unstructured":"Harmelin-Vivien, M. L. & Laboute, P. Catastrophic impact of hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia). Coral Reefs 5, 55\u201362 (1986).","journal-title":"Coral Reefs"},{"key":"64779_CR19","doi-asserted-by":"publisher","first-page":"914","DOI":"10.1007\/BF02798650","volume":"29","author":"M Wilson","year":"2006","unstructured":"Wilson, M., Meyers, S. D. & Luther, M. E. Changes in the circulation of Tampa Bay due to Hurricane Frances as recorded by ADCP measurements and reproduced with a numerical ocean model. Estuaries Coasts 29, 914\u2013918 (2006).","journal-title":"Estuaries Coasts"},{"key":"64779_CR20","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1007\/s00227-018-3459-z","volume":"166","author":"PJ Edmunds","year":"2019","unstructured":"Edmunds, P. J., Tsounis, G., Boulon, R. & Bramanti, L. Acute effects of back-to-back hurricanes on the underwater light regime of a coral reef. Mar. Biol. 166, 20 (2019).","journal-title":"Mar. Biol."},{"key":"64779_CR21","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1111\/j.1442-9993.1998.tb00733.x","volume":"23","author":"GP Jones","year":"1998","unstructured":"Jones, G. P. & Syms, C. Disturbance, habitat structure and the ecology of fishes on coral reefs. Austral Ecol. 23, 287\u2013297 (1998).","journal-title":"Austral Ecol."},{"key":"64779_CR22","doi-asserted-by":"publisher","first-page":"1229","DOI":"10.1017\/S0025315406014238","volume":"86","author":"L Wantiez","year":"2006","unstructured":"Wantiez, L., Chateau, O. & Le Mouellic, S. Initial and mid-term impacts of cyclone Erica on coral reef fish communities and habitat in the South Lagoon Marine Park of New Caledonia. J. Mar. Biol. Assoc. U. K. 86, 1229\u20131236 (2006).","journal-title":"J. Mar. Biol. Assoc. U. K."},{"key":"64779_CR23","unstructured":"Rousseau, Y., Galzin, R. & Mar\u00e9chal, J.-P. Impact of hurricane Dean on coral reef benthic and fish structure of Martinique, French West Indies. Cybium 34, (2010)."},{"key":"64779_CR24","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/0022-0981(92)90094-Q","volume":"161","author":"AJ Underwood","year":"1992","unstructured":"Underwood, A. J. Beyond BACI: the detection of environmental impacts on populations in the real, but variable, world. J. Exp. Mar. Biol. Ecol. 161, 145\u2013178 (1992).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"64779_CR25","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-50525-1","volume":"9","author":"A Brante","year":"2019","unstructured":"Brante, A. et al. Post-disturbance genetic changes: the impact of the 2010 mega-earthquake and tsunami on Chilean sandy beach fauna. Sci. Rep. 9, 14239 (2019).","journal-title":"Sci. Rep."},{"key":"64779_CR26","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.1111\/maec.12377","volume":"37","author":"S Hirase","year":"2016","unstructured":"Hirase, S., Ikeda, M., Hayasaka, S., Iwasaki, W. & Kijima, A. Stability of genetic diversity in an intertidal goby population after exposure to tsunami disturbance. Mar. Ecol. 37, 1161\u20131167 (2016).","journal-title":"Mar. Ecol."},{"key":"64779_CR27","doi-asserted-by":"publisher","DOI":"10.1038\/srep44375","volume":"7","author":"O Miura","year":"2017","unstructured":"Miura, O. et al. Ecological and genetic impact of the 2011 Tohoku earthquake tsunami on intertidal mud snails. Sci. Rep. 7, 44375 (2017).","journal-title":"Sci. Rep."},{"key":"64779_CR28","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1086\/668831","volume":"181","author":"JJ Apodaca","year":"2013","unstructured":"Apodaca, J. J., Trexler, J. C., Jue, N. K., Schrader, M. & Travis, J. Large-scale natural disturbance alters genetic population structure of the sailfin molly, Poecilia latipinna. Am. Nat. 181, 254\u2013263 (2013).","journal-title":"Am. Nat."},{"key":"64779_CR29","doi-asserted-by":"publisher","first-page":"888","DOI":"10.1017\/S0031182013000097","volume":"140","author":"AM Coile","year":"2013","unstructured":"Coile, A. M. & Sikkel, P. C. An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140, 888\u2013896 (2013).","journal-title":"Parasitology"},{"key":"64779_CR30","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1007\/978-3-030-17385-2_10","volume-title":"Parasitic Crustacea","author":"Paul C. Sikkel","year":"2019","unstructured":"Sikkel, P. C. & Welicky, R. L. The Ecological Significance of Parasitic Crustaceans. in Parasitic Crustacea: State of Knowledge and Future Trends (eds. Smit, N. J., Bruce, N. L. & Hadfield, K. A.) 421\u2013477, https:\/\/doi.org\/10.1007\/978-3-030-17385-2_10 (Springer International Publishing, 2019)."},{"key":"64779_CR31","doi-asserted-by":"publisher","first-page":"3875","DOI":"10.1007\/s00436-014-4090-7","volume":"113","author":"AM Coile","year":"2014","unstructured":"Coile, A. M., Welicky, R. L. & Sikkel, P. C. Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol. Res. 113, 3875\u20133880 (2014).","journal-title":"Parasitol. Res."},{"key":"64779_CR32","doi-asserted-by":"crossref","unstructured":"Smit, N. J. & Davies, A. J. The curious life-style of the parasitic stages of gnathiid Isopods. in Advances in Parasitology vol. 58, 289\u2013391 (Elsevier, 2004).","DOI":"10.1016\/S0065-308X(04)58005-3"},{"key":"64779_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3800\/pbr.2.1","volume":"2","author":"K Tanaka","year":"2007","unstructured":"Tanaka, K. Life history of gnathiid isopods-current knowledge and future directions. Plankton Benthos Res. 2, 1\u201311 (2007).","journal-title":"Plankton Benthos Res."},{"key":"64779_CR34","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1007\/s10750-007-0772-9","volume":"592","author":"MC Verweij","year":"2007","unstructured":"Verweij, M. C. & Nagelkerken, I. Short and long-term movement and site fidelity of juvenile Haemulidae in back-reef habitats of a Caribbean embayment. Hydrobiologia 592, 257\u2013270 (2007).","journal-title":"Hydrobiologia"},{"key":"64779_CR35","doi-asserted-by":"publisher","first-page":"211","DOI":"10.3354\/meps08714","volume":"415","author":"C Hammerschlag-Peyer","year":"2010","unstructured":"Hammerschlag-Peyer, C. & Layman, C. Intrapopulation variation in habitat use by two abundant coastal fish species. Mar. Ecol. Prog. Ser. 415, 211\u2013220 (2010).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"64779_CR36","doi-asserted-by":"publisher","first-page":"275","DOI":"10.3354\/meps09093","volume":"427","author":"S Hitt","year":"2011","unstructured":"Hitt, S., Pittman, S. & Nemeth, R. Diel movements of fishes linked to benthic seascape structure in a Caribbean coral reef ecosystem. Mar. Ecol. Prog. Ser. 427, 275\u2013291 (2011).","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"64779_CR37","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/j.fishres.2011.08.013","volume":"112","author":"DT Topping","year":"2011","unstructured":"Topping, D. T. & Szedlmayer, S. T. Home range and movement patterns of red snapper (Lutjanus campechanus) on artificial reefs. Fish. Res. 112, 77\u201384 (2011).","journal-title":"Fish. Res."},{"key":"64779_CR38","doi-asserted-by":"publisher","first-page":"e96028","DOI":"10.1371\/journal.pone.0096028","volume":"9","author":"SJ Pittman","year":"2014","unstructured":"Pittman, S. J. et al. Fish with chips: tracking reef fish movements to evaluate size and connectivity of Caribbean marine protected areas. PLoS ONE 9, e96028 (2014).","journal-title":"PLoS ONE"},{"key":"64779_CR39","doi-asserted-by":"publisher","first-page":"475","DOI":"10.5343\/bms.2016.1021","volume":"93","author":"P Sikkel","year":"2017","unstructured":"Sikkel, P. et al. Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull. Mar. Sci. 93, 475\u2013489 (2017).","journal-title":"Bull. Mar. Sci."},{"key":"64779_CR40","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1111\/j.1095-8312.2008.00997.x","volume":"94","author":"L Nagel","year":"2008","unstructured":"Nagel, L., Montgomerie, R. & Lougheed, S. C. Evolutionary divergence in common marine ectoparasites Gnathia spp. (Isopoda: Gnathiidae) on the Great Barrier Reef: phylogeography, morphology, and behaviour: evolutionary divergence in gnathiids. Biol. J. Linn. Soc. 94, 569\u2013587 (2008).","journal-title":"J. Linn. Soc."},{"key":"64779_CR41","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1086\/BBLv216n3p373","volume":"216","author":"AL Shanks","year":"2009","unstructured":"Shanks, A. L. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216, 373\u2013385 (2009).","journal-title":"Biol. Bull."},{"key":"64779_CR42","doi-asserted-by":"publisher","first-page":"47","DOI":"10.11646\/zootaxa.3381.1.3","volume":"3381","author":"C Farquharson","year":"2012","unstructured":"Farquharson, C., Smit, N. J. & Sikkel, P. C. Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the eastern Caribbean. Zootaxa 3381, 47 (2012).","journal-title":"Zootaxa"},{"key":"64779_CR43","doi-asserted-by":"publisher","first-page":"3425","DOI":"10.1175\/MWR-D-18-0078.1","volume":"146","author":"PJ Klotzbach","year":"2018","unstructured":"Klotzbach, P. J. et al. The extremely active 2017 North Atlantic hurricane season. Mon. Weather Rev. 146, 3425\u20133443 (2018).","journal-title":"Mon. Weather Rev."},{"key":"64779_CR44","doi-asserted-by":"publisher","unstructured":"Gochfeld, D. J. et al. Impacts of hurricanes Irma and Maria on coral reef sponge communities in St. Thomas, U.S. Virgin Islands. Estuaries Coasts https:\/\/doi.org\/10.1007\/s12237-020-00694-4 (2020).","DOI":"10.1007\/s12237-020-00694-4"},{"key":"64779_CR45","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.ijppaw.2016.05.003","volume":"5","author":"JM Artim","year":"2016","unstructured":"Artim, J. M. & Sikkel, P. C. Comparison of sampling methodologies and estimation of population parameters for a temporary fish ectoparasite. Int. J. Parasitol. Parasites Wildl. 5, 145\u2013157 (2016).","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"64779_CR46","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1007\/s10126-005-0017-8","volume":"7","author":"L Podsiadlowski","year":"2005","unstructured":"Podsiadlowski, L. & Bartolomaeus, T. Organization of the mitochondrial genome of mantis shrimp Pseudosquilla ciliata (Crustacea: Stomatopoda). Mar. Biotechnol. 7, 618\u2013624 (2005).","journal-title":"Mar. Biotechnol."},{"key":"64779_CR47","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-13-134","volume":"13","author":"J Ye","year":"2012","unstructured":"Ye, J. et al. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134 (2012).","journal-title":"BMC Bioinformatics"},{"issue":"4","key":"64779_CR48","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1093\/bib\/bbx108","volume":"20","author":"Kazutaka Katoh","year":"2017","unstructured":"Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. https:\/\/doi.org\/10.1093\/bib\/bbx108 (2017).","journal-title":"Briefings in Bioinformatics"},{"key":"64779_CR49","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1093\/molbev\/msw054","volume":"33","author":"S Kumar","year":"2016","unstructured":"Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870\u20131874 (2016).","journal-title":"Mol. Biol. Evol."},{"key":"64779_CR50","doi-asserted-by":"publisher","first-page":"2333","DOI":"10.1007\/s00227-012-2018-2","volume":"159","author":"Y Ota","year":"2012","unstructured":"Ota, Y., Hoshino, O., Hirose, M., Tanaka, K. & Hirose, E. Third-stage larva shifts host fish from teleost to elasmobranch in the temporary parasitic isopod, Gnathia trimaculata (Crustacea; Gnathiidae). Mar. Biol. 159, 2333\u20132347 (2012).","journal-title":"Mar. Biol."},{"key":"64779_CR51","doi-asserted-by":"publisher","first-page":"117693430500100","DOI":"10.1177\/117693430500100003","volume":"1","author":"L Excoffier","year":"2005","unstructured":"Excoffier, L., Laval, G. & Schneider, S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinforma. 1, 117693430500100 (2005).","journal-title":"Evol. Bioinforma."},{"key":"64779_CR52","doi-asserted-by":"publisher","first-page":"e281","DOI":"10.7717\/peerj.281","volume":"2","author":"ZN Kamvar","year":"2014","unstructured":"Kamvar, Z. N., Tabima, J. F. & Gr\u00fcnwald, N. J. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and\/or sexual reproduction. PeerJ 2, e281 (2014).","journal-title":"PeerJ"},{"key":"64779_CR53","doi-asserted-by":"publisher","first-page":"1657","DOI":"10.1046\/j.1365-294x.2000.01020.x","volume":"9","author":"M Clement","year":"2000","unstructured":"Clement, M., Posada, D. & Crandall, K. A. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657\u20131659 (2000).","journal-title":"Mol. Ecol."},{"key":"64779_CR54","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1093\/bioinformatics\/btv636","volume":"32","author":"A M\u00farias dos Santos","year":"2016","unstructured":"M\u00farias dos Santos, A., Cabezas, M. P., Tavares, A. I., Xavier, R. & Branco, M. tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics 32, 627\u2013628 (2016).","journal-title":"Bioinformatics"},{"key":"64779_CR55","first-page":"32","volume":"26","author":"MJ Anderson","year":"2001","unstructured":"Anderson, M. J. A new method for non-parametric multivariate analysis of variance: non-parametric manova for ecology. Austral Ecol. 26, 32\u201346 (2001).","journal-title":"Austral Ecol."},{"key":"64779_CR56","first-page":"5","volume":"2","author":"J Oksanen","year":"2019","unstructured":"Oksanen, J. et al. vegan: Community Ecology Package. R package version 2, 5\u20134 (2019).","journal-title":"R package version"},{"key":"64779_CR57","first-page":"65","volume":"6","author":"S Holm","year":"1979","unstructured":"Holm, S. A simple sequentially rejective multiple test procedure. Scand J Stat. 6, 65\u201370 (1979).","journal-title":"Scand J Stat."},{"key":"64779_CR58","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1093\/jhered\/esh074","volume":"95","author":"S Piry","year":"2004","unstructured":"Piry, S. et al. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95, 536\u2013539 (2004).","journal-title":"J. Hered."},{"key":"64779_CR59","doi-asserted-by":"publisher","first-page":"9197","DOI":"10.1073\/pnas.94.17.9197","volume":"94","author":"B Rannala","year":"1997","unstructured":"Rannala, B. & Mountain, J. L. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. 94, 9197\u20139201 (1997).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"64779_CR60","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1046\/j.1365-294X.2004.02008.x","volume":"13","author":"D Paetkau","year":"2004","unstructured":"Paetkau, D., Slade, R., Burden, M. & Estoup, A. Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol. Ecol. 13, 55\u201365 (2004).","journal-title":"Mol. Ecol."},{"key":"64779_CR61","doi-asserted-by":"publisher","first-page":"e1285","DOI":"10.1371\/journal.pone.0001285","volume":"2","author":"S Steinfartz","year":"2007","unstructured":"Steinfartz, S. et al. Genetic impact of a severe el ni\u00f1o event on Gal\u00e1pagos marine iguanas (Amblyrhynchus cristatus). PLoS ONE 2, e1285 (2007).","journal-title":"PLoS ONE"},{"key":"64779_CR62","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1111\/j.1558-5646.1988.tb02519.x","volume":"42","author":"JC Trexler","year":"1988","unstructured":"Trexler, J. C. Hierarchical organization of genetic variation in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). Evolution 42, 1006\u20131017 (1988).","journal-title":"Evolution"},{"key":"64779_CR63","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1126\/science.289.5487.2068","volume":"289","author":"DR Easterling","year":"2000","unstructured":"Easterling, D. R. Climate extremes: observations, modeling, and impacts. Science 289, 2068\u20132074 (2000).","journal-title":"Science"},{"key":"64779_CR64","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1111\/gcb.13593","volume":"23","author":"AJ Cheal","year":"2017","unstructured":"Cheal, A. J., MacNeil, M. A., Emslie, M. J. & Sweatman, H. The threat to coral reefs from more intense cyclones under climate change. Glob. Change Biol. 23, 1511\u20131524 (2017).","journal-title":"Glob. Change Biol."},{"key":"64779_CR65","doi-asserted-by":"publisher","first-page":"e1004551","DOI":"10.1371\/journal.pgen.1004551","volume":"10","author":"HA Orr","year":"2014","unstructured":"Orr, H. A. & Unckless, R. L. The population genetics of evolutionary rescue. PLoS Genet. 10, e1004551 (2014).","journal-title":"PLoS Genet."},{"key":"64779_CR66","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1111\/j.1558-5646.1991.tb04333.x","volume":"45","author":"M Lynch","year":"1991","unstructured":"Lynch, M. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45, 622\u2013629 (1991).","journal-title":"Evolution"},{"key":"64779_CR67","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1038\/hdy.2010.165","volume":"106","author":"V Bourret","year":"2011","unstructured":"Bourret, V., O\u2019Reilly, P. T., Carr, J. W., Berg, P. R. & Bernatchez, L. Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees. Heredity 106, 500\u2013510 (2011).","journal-title":"Heredity"},{"key":"64779_CR68","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1093\/icb\/icp033","volume":"49","author":"RM Overstreet","year":"2009","unstructured":"Overstreet, R. M., Jovonovich, J. & Ma, H. Parasitic crustaceans as vectors of viruses, with an emphasis on three penaeid viruses. Integr. Comp. Biol. 49, 127\u2013141 (2009).","journal-title":"Integr. Comp. Biol."},{"key":"64779_CR69","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1016\/j.ijpara.2012.11.012","volume":"43","author":"LM Curtis","year":"2013","unstructured":"Curtis, L. M., Grutter, A. S., Smit, N. J. & Davies, A. J. Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Int. J. Parasitol. 43, 361\u2013370 (2013).","journal-title":"Int. J. Parasitol."},{"key":"64779_CR70","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1007\/978-3-030-17385-2_7","volume-title":"Parasitic Crustacea","author":"Kerry A. Hadfield","year":"2019","unstructured":"Hadfield, K. A. & Smit, N. J. Parasitic Crustacea as Vectors. in Parasitic Crustacea: State of Knowledge and Future Trends (eds. Smit, N. J., Bruce, N. L. & Hadfield, K. A.) 331\u2013342, https:\/\/doi.org\/10.1007\/978-3-030-17385-2_7 (Springer International Publishing, 2019)."},{"key":"64779_CR71","doi-asserted-by":"publisher","first-page":"1737","DOI":"10.1126\/science.1152509","volume":"318","author":"O Hoegh-Guldberg","year":"2007","unstructured":"Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737\u20131742 (2007).","journal-title":"Science"},{"key":"64779_CR72","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1126\/science.1159196","volume":"321","author":"KE Carpenter","year":"2008","unstructured":"Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560\u2013563 (2008).","journal-title":"Science"},{"key":"64779_CR73","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1130\/0091-7613(1995)023<0004:RDDTLD>2.3.CO;2","volume":"23","author":"P Blanchon","year":"1995","unstructured":"Blanchon, P. & Shaw, J. Reef drowning during the last deglaciation: evidence for catastrophic sea-level rise and ice-sheet collapse. Geology 23, 4\u20138 (1995).","journal-title":"Geology"},{"key":"64779_CR74","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1007\/s00338-019-01835-3","volume":"38","author":"PC Sikkel","year":"2019","unstructured":"Sikkel, P. C. et al. Changes in abundance of fish-parasitic gnathiid isopods associated with warm-water bleaching events on the northern Great Barrier Reef. Coral Reefs 38, 721\u2013730 (2019).","journal-title":"Coral Reefs"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-64779-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-64779-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-64779-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,6]],"date-time":"2022-12-06T11:28:20Z","timestamp":1670326100000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-64779-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,26]]},"references-count":74,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["64779"],"URL":"https:\/\/doi.org\/10.1038\/s41598-020-64779-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,26]]},"assertion":[{"value":"6 January 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 March 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 May 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"8649"}}