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Comparing genetic connectivity among Dungeness crab (Cancer magister) inhabiting Puget Sound and coastal Washington

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Abstract

Understanding connectivity of marine organisms is necessary for determining the appropriate scale of conservation and management strategies. For species that inhabit both the coastal ocean and partially enclosed water bodies (i.e., estuaries or fjords), this information is even more critical since estuaries and fjords are often characterized by hydrological complexities which can limit dispersal potential and promote population subdivision. In this study, genetic connectivity of Dungeness crab Cancer magister in Puget Sound and coastal Washington, USA, was examined to test the hypothesis of genetic structure in partially enclosed versus open environments. Dungeness crab that were sampled at five sites in Puget Sound in 2015 and three sites in coastal Washington in 2014 were genotyped at ten microsatellite loci. We observed similar levels of heterozygosity and allelic richness within Puget Sound and coastal Washington. Pairwise F ST estimates indicated that Hood Canal was significantly differentiated from other Puget Sound sites, except Nisqually, suggesting larval retention within the Hood Canal basin. No evidence for significant genetic differentiation was found among the four remaining Puget Sound sites or among the three coastal sites. Analysis of molecular variance indicated that, in aggregate, Puget Sound sites significantly differed from coastal sites. On a site by site basis, we found evidence for significant differentiation between three sites in Puget Sound and coastal Washington. Based upon the observed patterns of genetic differentiation, our findings did not support our hypothesis of restricted genetic connectivity within Puget Sound, with the exception of Hood Canal. However, our results demonstrate that there is stronger genetic connectivity within Puget Sound and coastal Washington than between these two areas.

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References

  • Babson AL, Kawase M, MacCready P (2006) Seasonal and interannual variability in the circulation of Puget Sound, Washington: a box model study. Atmos Ocean 44:29–45

    Article  Google Scholar 

  • Beacham TD, Supernault J, Miller KM (2008) Population structure of Dungeness crab (Cancer magister) in British Columbia. J Shellfish Res 27:901–906

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05: logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, populations, interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France

  • Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315

    Article  Google Scholar 

  • Benestan L, Moore JS, Sutherland BJG, Le Luyer J, Maaroufi H, Rougeux C, Normandeau E, Rycroft N, Atema J, Harris LN, Tallman RF, Greenwood SJ, Clark KF, Bernatchez (2016) Sex matters in massive parallel sequencing: evidence for biases in genetic parameter estimation and investigation of sex determination systems. bioRxiv. doi:10.1101/096065

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Bradbury IR, Campana SE, Bentzen P (2007) Low genetic connectivity in an estuarine fish with pelagic larvae. Can J Fish Aquat Sci 65:147–158

    Article  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA, Vetter RD (2002) Population structure of copper rockfish (Sebastes caurinus) reflects postglacial colonization and contemporary patterns of larval dispersal. Can J Fish Aquat Sci 59:1374–1384

    Article  CAS  Google Scholar 

  • Buonaccorsi VP, Kimbrell CA, Lynn EA, Vetter RD (2005) Limited realized dispersal and introgressive hybridization influence genetic structure and conservation strategies for brown rockfish, Sebastes auriculatus. Conserv Genet 6:697–713

    Article  Google Scholar 

  • Camara MD, Vadopalas B (2009) Genetic aspects of restoring Olympia oyster and other native bivalves: balancing the need for action, good intentions, and the risks of making things worse. J Shellfish Res 28:121–145

    Article  Google Scholar 

  • Cannon GA (1983) An overview of circulation in the Puget Sound estuarine system. NOAA Technical Memorandum, ERL PMEL 48:30

    Google Scholar 

  • Carr M, Syms C (2006) Recruitment. In: Allen LG, Pondella DJ, Horn MH (eds) The ecology of marine fishes: California and adjacent waters. University of California Press, Berkeley, pp 411–427

    Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  Google Scholar 

  • Chust G, Villarino A, Chenuil A, Irigoien X, Bizsel N, Bod A, Broms C, Claus S, Fernández de Puelles ML, Fonda-Umani S, Hoarau G, Mazzocchi MG, Mozetič P, Vandepitte L, Veríssimo H, Zervoudaki S, Borja A (2016) Dispersal similarly shapes both population genetics and community patterns in the marine realm. Sci Rep 6:28730

    Article  CAS  Google Scholar 

  • Ciannelli L, Knutsen H, Olsen EM, Espeland SH, Asplin L, Jelmert A, Knutsen JA, Stenseth NC (2010) Small-scale genetic structure in a marine population in relation to water circulation and egg characteristics. Ecology 91:2918–2930

    Article  Google Scholar 

  • Collier P (1983) Movement and growth of post-larval Dungeness crabs, Cancer magister, in the San Francisco area. Calif Fish Game Fish Bull 172:125–134

    Google Scholar 

  • Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • Cowen R, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE (2007) Population connectivity in marine systems an overview. Oceanography 20:14–21

    Article  Google Scholar 

  • Cunningham KM, Canino MF, Spies IB, Hauser L (2009) Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean. Can J Fish Aquat Sci 66:153–166

    Article  CAS  Google Scholar 

  • Diamond N, Hankin DG (1985) Movements of adult female Dungeness crabs (Cancer magister) in northern California based on tag recoveries. Can J Fish Aquat Sci 42:919–926

    Article  Google Scholar 

  • Dinnel PA, Armstrong DA, McMillian RO (1993) Evidence for multiple recruitment-cohorts of Puget Sound Dungeness crab, Cancer magister. Mar Biol 115:53–63

    Article  Google Scholar 

  • Dinnel P, Dolph I, Elder D, Woodward C, Woodard T (2011) Restoration of the native oyster in Fidalgo Bay, Washington—year nine report. Skagit County Marine Resource Committee, Mount Vernon

    Google Scholar 

  • Doyle M, Picquelle SJ, Mier KL, Spillane MC, Bond NA (2009) Larval fish abundance and physical forcing in the Gulf of Alaska, 1981–2003. Prog Oceanogr 80:163–187

    Article  Google Scholar 

  • Ebbesmeyer CC, Word JQ, Barnes CA (1988) Puget Sound: A fjord system homogenized with water recycled over sills by tidal mixing. In: Kjerfve B (ed) Hydrodynamics of estuaries 2: Estuarine case studies. CRC Press, Boca Rotan, pp 17–29

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    CAS  Google Scholar 

  • Falk DA, Richards CM, Montalvo AM, Knapp EE (2006) Population and ecological genetic in restoration ecology. In: Falk DA, Palmer MA, Zedler JB (eds) Foundations of restoration ecology. Island Press, Washington, D.C., pp 14–42

    Google Scholar 

  • Fisher JL (2006) Seasonal timing and duration of brachyuran larvae in a high-latitude fjord. Mar Ecol Prog Ser 323:213–222

    Article  Google Scholar 

  • Froelich HE, Essington TE, Beaudreau AH, Levin PS (2014) Movement patterns and distributional shifts of Dungeness crab (Metacarcinus magister) and English sole (Parophrys vetulus) during seasonal hypoxia. Estaur Coast 37:449–460

    Article  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  Google Scholar 

  • Gillanders BM, Elsdon TS, Roughan M (2012) Connectivity of Estuaries. In: Heip CHR, Middelburg JJ, Philippart CJM (eds) Treatise on estuarine and coastal science, volume 7: functioning of ecosystems at the land–ocean interface, vol 7. Elsevier, London, pp 119–142

    Google Scholar 

  • Gotshall DW (1978) Northern California Dungeness crab, Cancer magister, movements as shown by tagging. Calif Fish Game 64:234–254

    Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9. 3, a program to estimate and test gene diversities and fixation indices. Lausanne University, Lausanne

    Google Scholar 

  • Gregg MC, Pratt LJ (2010) Flow and hydraulics near the sill of Hood Canal, a strongly sheared, continuously stratified fjord. J Phys Oceanogr 40:1087–1105

    Article  Google Scholar 

  • Hildenbrand K, Gladics AJ, Eder R (2011) Adult male Dungeness crab (Metacarcinus magister) movements near Reedsport, Oregon from a fisheries collaborative mark-recapture study. Oregon Wave Energy Trust and the Oregon Dungeness Crab Commission, Oregon

    Google Scholar 

  • Ivanova NV, deWaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002

    Article  CAS  Google Scholar 

  • Iwamoto E, Ford MJ, Gustafson RG (2004) Genetic population structure of Pacific hake, Merluccius productus, in the Pacific Northwest. Environ Biol Fish 69:187–199

    Article  Google Scholar 

  • Jamieson GS, Phillips A (1993) Megalopal spatial distribution and stock separation in Dungeness crab (Cancer magister). Can J Fish Aquat Sci 50:416–429

    Article  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  Google Scholar 

  • Kalinowski ST (2009) How well do evolutionary trees describe genetic relationships among populations? Heredity 102:506–513

    Article  CAS  Google Scholar 

  • Kaukinen KH, Supernault KJ, Miller KM (2004) Enrichment of tetranucleotide microsatellite loci from invertebrate species. J Shellfish Res 23:621–626

    Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    CAS  Google Scholar 

  • Knutsen H, Jorde PE, André C, Stenseth NC (2003) Finescaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394

    Article  CAS  Google Scholar 

  • Knutsen H, Olsen EM, Jorde PE, Espeland SH, André C, Stenseth NC (2011) Are low but statistically significant levels of genetic differentiation in marine fishes ‘biologically meaningful?’ A case study of coastal Atlantic cod. Mol Ecol 20:768–783

    Article  CAS  Google Scholar 

  • Kumar G, Kocour M (2016) Applications of next-generation sequencing in fisheries research: a review. Fish Res 186:11–22

    Article  Google Scholar 

  • Lough R (1976) Larval dynamics of the Dungeness crab, Cancer magister, off the central Oregon coast, 1970–71. Fish B NOAA 74:353–376

    Google Scholar 

  • Love MS, Yoklavich M, Thorsteinson L (2002) The rockfishes of the Northeast Pacific. University of California Press, Berkeley

    Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 15:3038–3051

    Article  Google Scholar 

  • McFarlane GA, Beamish RJ (1985) Biology and fishery of Pacific whiting, Merluccius productus in the Strait of Georgia. Mar Fish Rev 47:23–34

    Google Scholar 

  • McMillan RO, Armstrong DA, Dinnel PA (1995) Comparison of intertidal habitat use and growth rates of two northern Puget Sound cohorts of 0+ age Dungeness Crab, Cancer magister. Estuaries 18:390–398

    Article  Google Scholar 

  • Meirmans PG (2006) Using AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402

    Article  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • O’Malley K, Corbett K, Beacham T, Jacobson D, Jackson T, Roegner G (2017) Genetic connectivity of Dungeness crab (Cancer magister) across oceanographic regimes. J Shellfish Res (in review)

  • Pacific States Marine Fisheries Commission (2014) Revised pre-season testing protocol for the tri-state coastal Dungeness Crab Commercial Fishery. http://www.psmfc.org/crab/2013-2014%20files/2014preseasontesting.pdf. Accessed 16 July 2016

  • Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158

    Article  Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:34–68

    Article  Google Scholar 

  • Pante E, Simon-Bouhet B (2013) Marmap: a package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One 8:e73051

    Article  CAS  Google Scholar 

  • Parker MS, Jumars PA, LeClair L (2003) Population genetics of two bivalve species (Prototheca satminea and macoma balthica) in Puget Sound, Washington. J Shellfish Res 22:681–688

    Google Scholar 

  • Pritchard C, Shanks A, Rimler R, Oates M, Rumrill S (2015) The Olympia oyster Ostrea lurida: recent advances in natural history, ecology, and restoration. J Shellfish Res 34:259–271

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 23 Sept 2016

  • Rasmuson L (2013) The biology, ecology and fishery of the Dungeness crab, Cancer magister. Adv Mar Biol 65:95–148

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exacts tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Reiss H, Haorau G, Dicky-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10:361–395

    Article  Google Scholar 

  • Rogers LA, Olsen EM, Knutsen H, Stenseth NC (2014) Habitat effects on population connectivity in a coastal seascape. Mar Ecol Prog Ser 511:153–163

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

    Article  Google Scholar 

  • Selkoe KA, D’Aola CC, Crandall ED, Iacchei M, Liggins L, Purtiz JB, von der Heyden S, Toonen RJ (2016) A decade of seascape genetics: contributions to basic and applied marine connectivity. Mol Ecol Prog Ser 554:1–19

    Article  Google Scholar 

  • Shanks AL (2013) Atmospheric forcing drives recruitment variation in the Dungeness crab (Cancer magister), revisited. Fish Oceanogr 22:263–272

    Article  Google Scholar 

  • Shanks AL, Roegner GC (2007) Recruitment limitation in Dungeness crab is driven by variation in atmospheric forcing. Ecology 88:1726–1737

    Article  Google Scholar 

  • Shanks AL, Roegner GC, Miller JA (2010) Using megalopae abundance to predict future commercial catches of Dungeness crabs (Cancer magister) in Oregon. Cal Coop Ocean Fish 51:1–13

    Google Scholar 

  • Smith BD, Jamieson GS (1991) Movement, spatial distribution, and mortality of male and female Dungeness crab Cancer magister near Tofino, British Columbia. Fish Bull 89:137–148

    Google Scholar 

  • Snow C, Wagner E (1965) Tagging of Dungeness crabs with spaghetti and dart tags. Fish Commun Oreg 4629:5–13

    Google Scholar 

  • Stick DA (2011) Identification of optimal broodstock for Pacific Northwest oysters. Dissertation, Oregon State University

  • Toonen RJ, Harris ML, Gosberg R (2004) Isolation and characterization of polymorphic microsatellite loci from the Dungeness crab Cancer magister. Mol Ecol Notes 4:30–32

    Article  CAS  Google Scholar 

  • Vadopalas B, Leclair LL, Bentzen P (2004) Microsatellite and allozyme analyses reveal few genetic differences among spatially distinct aggregations of geoduck clams (Panopea abrupta, Conrad 1849). J Shellfish Res 23:693–706

    Google Scholar 

  • Wainwright TC, Armstrong DA (1993) Growth patterns in the Dungeness crab (Cancer magister): synthesis of data and comparison of models. J Crustac Biol 13:36–50

    Article  Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  Google Scholar 

  • Weersing KA (2007) Population genetics, larval dispersal, and demographic connectivity in marine systems. Thesis, University of Hawaii

  • Weir BS (1996) Genetic data analysis II. Sinauer Associates, Sunderland

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 23:114–138

    Google Scholar 

  • Yang Z, Wang T (2013) Tidal residual eddies and their effect on water exchange in Puget Sound. Ocean Dynam 63:995–1009

    Article  Google Scholar 

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Acknowledgements

This report was prepared by Oregon Sea Grant under grant number NA14OAR4170064 (CFDA No. 11.417) (Project Number R/RCF-33) from the National Oceanic and Atmospheric Administration’s National Sea Grant College Program, US Department of Commerce, and by appropriations made by the Oregon State Legislature. The statements, findings, conclusions, and recommendations are those of the authors and do not necessarily reflect the views of these funders. This research was also funded by the Hatfield Marine Science Center Bill Wick Marine Fisheries Award. We thank the Washington Department of Fish and Wildlife, the Washington commercial Dungeness crab fishing fleet, and the Suquamish, Swinomish, and Nisqually Tribes for their cooperation and assistance in sampling of Dungeness crab. We would also like to thank Dr. David Armstrong (Marine Biology, University of Washington) for his comments on an earlier version of this manuscript.

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Correspondence to Tyler M. Jackson.

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All animals were sampled in accordance with Oregon State University and national ethical standards. Permission for sampling was granted through the Washington Department of Fish and Wildlife, as well as the Suquamish, Swinomish, and Nisqually Tribes.

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The authors have no conflict of interest pertaining to this study, and consent was given by Tyler M. Jackson, Kathleen G. O’Malley, and those who assisted with sampling.

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Responsible editor: O. Puebla.

Reviewed by L. Benestan and G. Winans.

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Jackson, T.M., O’Malley, K.G. Comparing genetic connectivity among Dungeness crab (Cancer magister) inhabiting Puget Sound and coastal Washington. Mar Biol 164, 123 (2017). https://doi.org/10.1007/s00227-017-3152-7

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