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The role of cryptic dispersal in shaping connectivity patterns of marine populations in a changing world

Published online by Cambridge University Press:  02 March 2017

Andrew A. David  and
Benjamin R. Loveday
Andrew A. David*
Affiliation:
Department of Biology, Clarkson University, Potsdam, NY – 13699, USA
Benjamin R. Loveday
Affiliation:
Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UK
*
Correspondence should be addressed to: A.A. David Department of Biology, Clarkson University, 8 Clarkson Avenue, Potsdam NY 13699, Box 5805, USA email: [email protected]
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Abstract

Genetic connectivity directly shapes the demographic profile of marine species, and has become one of the most intensely researched areas in marine ecology. More importantly, it has changed the way we design and describe Marine Protected Areas across the world. Population genetics is the preferred tool when measuring connectivity patterns, however, these methods often assume that dispersal patterns are (1) natural and (2) follow traditional metapopulation models. In this short review, we formally introduce the phenomenon of cryptic dispersal, where multiple introductory events can undermine these assumptions, resulting in grossly inaccurate connectivity estimates. We also discuss the evolutionary consequences of cryptic dispersal and advocate for a cross-disciplinary approach that incorporates larval transport models into population genetic studies to provide a level of oceanographic realism that will result in more accurate estimates of dispersal. As globalized trade continues to expand, the rate of anthropogenic movement of marine organisms is also expected to increase and as such, integrated methods will be required to meet the inevitable conservation challenges that will arise from it.

Keywords

oceanographymodellinggeneticslarvaeintroductioninvasivespeciesaquaculturevectorballast
Type
Review
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 4 , June 2018 , pp. 647 - 655
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Ashton, G.V., Davidson, I.C., Geller, J. and Ruiz, G.M. (2016) Disentangling the biogeography of ship fouling: barnacles in the Northeast Pacific. Global Ecology and Biogeography 25, 739–750.CrossRefGoogle Scholar
Avise, J.C. (2009) Phylogeography: retrospect and prospect. Journal of Biogeography 36, 3–15.CrossRefGoogle Scholar
Baums, I.B., Paris, C.B. and Cherubin, L. (2006) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnology and Oceanography 51, 1969–1981.CrossRefGoogle Scholar
Buston, P.M. and D'Aloia, C.C. (2013) Marine ecology: reaping the benefits of local dispersal. Current Biology 23, R351–R353.CrossRefGoogle ScholarPubMed
Carlton, J.T. (1989) Man's role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conservation Biology 3, 265–273.CrossRefGoogle Scholar
Chu, K.H., Tam, P.F., Fung, C.H. and Chen, Q.C. (1997) A biological survey of ballast water in container ships entering Hong Kong. Hydrobiologia 352, 201–206.CrossRefGoogle Scholar
Ciotir, C. and Freeland, J. (2016) Cryptic intercontinental dispersal, commercial retailers, and the genetic diversity of native and non-native cattails (Typha spp.) in North America. Hydrobiologia 768, 137–150.CrossRefGoogle Scholar
Cope, R.C., Prowse, T.A.A., Ross, J.V., Wittmann, T.A. and Cassey, P. (2015) Temporal modelling of ballast water discharge and ship-mediated invasion risk to Australia. Royal Society Open Science 2, 150039.CrossRefGoogle ScholarPubMed
Cowen, R.K. and Sponaugle, S. (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.CrossRefGoogle ScholarPubMed
Crook, D.A., Lowe, W.H., Allendorf, F.W., Eros, T., Finn, D.S., Gillanders, B.M., Hadwen, W.L., Harrod, C., Hermoso, V., Jennings, S., Kilada, R.W., Nagelkerken, I., Hansen, M.M., Page, T.J., Riginos, C., Fry, B. and Hughes, J.M. (2015) Human effects on ecological connectivity in aquatic ecosystems: integrating scientific approaches to support management and mitigation. Science of the Total Environment 534, 52–64.CrossRefGoogle ScholarPubMed
Cumming, R.A., Nikula, R., Spencer, H.G. and Waters, J.M. (2014) Transoceanic genetic similarities of kelp-associated sea slug populations: long-distance dispersal via rafting? Journal of Biogeography 41, 2357–2370.CrossRefGoogle Scholar
Darling, J.A., Bagley, M.J., Roman, J., Tepolt, C.K. and Geller, G.B. (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Molecular Ecology 17, 4992–5007.CrossRefGoogle ScholarPubMed
Darling, J.A., Herborg, L.M. and Davidson, I.C. (2012) Intracoastal shipping drives patterns of regional population expansion by and invasive marine invertebrate. Ecology and Evolution 2, 2557–2566.CrossRefGoogle ScholarPubMed
David, A.A., Matthee, C.A., Loveday, B.R. and Simon, C.A. (2016) Predicting the dispersal potential of an invasive polychaete pest along a complex coastal biome. Integrative and Comparative Biology 56, 600–610.CrossRefGoogle ScholarPubMed
David, A.A. and Simon, C.A. (2014) The effect of temperature on larval development of two non-indigenous poecilogonous polychaetes (Annelida: Spionidae) with implications for life-history theory, establishment and range expansion. Journal of Experimental Marine Biology and Ecology 461, 20–30.CrossRefGoogle Scholar
Dawson, M.N., Gupta, A.S. and England, M.H. (2005) Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proceedings of the National Academy of Sciences USA 102, 11968–11973.CrossRefGoogle ScholarPubMed
Elton, C.S. (1958) The ecology of invasions by animals and plants. New York, NY: Springer. 181 pp.CrossRefGoogle Scholar
Galindo, H.M., Olson, D.B. and Palumbi, S.R. (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology 16, 1622–1626.CrossRefGoogle ScholarPubMed
Gilg, M.R. and Hilbish, T.J. (2003) The geography of marine larval dispersal: coupling genetics with fine-scale physical oceanography. Ecology 84, 2989–2998.CrossRefGoogle Scholar
Grosholz, E.D., Crafton, R.E., Fontana, R.E., Pasari, J.R., Williams, S.L. and Zabin, C.J. (2015) Aquaculture as a vector for marine invasions in California. Biological Invasions 17, 1471–1484.CrossRefGoogle Scholar
Haupt, T.M., Griffiths, C.L., Robinson, T.B. and Tonin, A.F.G. (2010) Oysters as vectors of marine alines, with notes on four introduced species associated with oyster farming in South Africa. African Zoology 45, 52–62.CrossRefGoogle Scholar
Hellberg, M.E. (2009) Gene flow and isolation among populations of marine animals. Annual Review of Ecology, Evolution and Systematics 40, 291–310.CrossRefGoogle Scholar
Hudson, J., Viard, F., Roby, C. and Rius, M. (2016) Anthropogenic transport of species across native ranges: unpredictable genetic and evolutionary consequences. Biology Letters 12, 20160620.CrossRefGoogle ScholarPubMed
Irwin, D.E. (2012) Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypic clustering. American Naturalist 180, 35–49.CrossRefGoogle ScholarPubMed
Johnson, M.S. (2000) Measuring and interpreting genetic structure to minimize the genetic risks of translocations. Aquaculture Research 31, 133–143.CrossRefGoogle Scholar
Karl, S.A., Toonen, R.J., Grant, W.S. and Bowen, B.W. (2012) Common misconceptions in molecular ecology: echoes of the modern synthesis. Molecular Ecology 21, 4171–4189.CrossRefGoogle ScholarPubMed
Kesaniemi, J.E., Hansen, B.W., Banta, G.T. and Knott, K.E. (2014) Chaotic genetic patchiness and high relatedness of a poecilogonous polychaete in a heterogenous estuarine landscape. Marine Biology 161, 2631–2644.CrossRefGoogle Scholar
Lejeusne, C., Saunier, A., Petit, N., Beguer, M., Otani, M., Carlton, J.T., Rico, C. and Green, A.J. (2014) High genetic diversity and absence of founder effects in a worldwide aquatic invader. Scientific Reports 4, 5808.CrossRefGoogle Scholar
Levin, L.A. (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46, 282–297.CrossRefGoogle ScholarPubMed
McDonald, K.M., Winter, D.J., Ashcroft, A.L. and Spencer, H.G. (2015) Phylogeography of the whelk genus Cominella (Gastropoda: Buccinidae) suggests long-distance counter-current dispersal of a direct developer. Biological Journal of the Linnaean Society 115, 315–332.Google Scholar
Metaxas, A. and Saunders, M. (2009) Quantifying the “Bio-” components in biophysical models of larval transport in marine benthic invertebrates: advances and pitfalls. Biological Bulletin 216, 257–272.CrossRefGoogle ScholarPubMed
Nikula, R., Spencer, H.G. and Waters, J.M. (2013) Passive rafting is a powerful driver of transoceanic gene-flow. Biology Letters 9, 20120821.CrossRefGoogle ScholarPubMed
Palumbi, S.R. (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, 146–158.CrossRefGoogle Scholar
Pringle, J.M. and Wares, J.P. (2007) Going against the flow: maintenance of alongshore variation in allele frequency in a coastal ocean. Marine Ecology Progress Series 335, 69–84.CrossRefGoogle Scholar
Reitzel, A.M., Darling, J.A., Sullivan, J.C. and Finnerty, J.R. (2008) Global population genetic structure of the starlet anemone Nematostella vectensis: multiple introductions and implications for conservation policy. Biological Invasions 10, 1197–1213.CrossRefGoogle Scholar
Reusch, T.B.H., Bolte, S., Sparwel, M., Moss, A.G.and Javidpour, J. (2010) Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world's most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Molecular Ecology 19, 2690–2699.CrossRefGoogle ScholarPubMed
Robinson, L.M., Elith, J., Hobday, A.J., Pearson, R.G., Kendall, B.E., Possingham, H.P. and Richardson, A.J. (2011) Pushing the limits in marine species distribution modelling: lessons from the land present challenges and opportunities. Global Ecology and Biogeography 20, 789–802.CrossRefGoogle Scholar
Roman, J. and Darling, J.A. (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution 22, 454–464.CrossRefGoogle ScholarPubMed
Selkoe, K.A., Henzler, C.M. and Gaines, S.D. (2008) Seascape genetics and the spatial ecology of marine populations. Fish and Fisheries 9, 363–377.CrossRefGoogle Scholar
Selkoe, K.A. and Toonen, R.J. (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series 436, 291–305.CrossRefGoogle Scholar
Shanks, A.L. (2009) Pelagic larval duration and dispersal distance revisited. Biological Bulletin 216, 373–385.CrossRefGoogle ScholarPubMed
Shchepetkin, A. and McWilliams, J. (2005) The Regional Oceanic Modeling System (ROMS): a split-explicit, free-surface, topography-following-coordinate ocean model. Ocean Model 9, 347–404.CrossRefGoogle Scholar
Siegel, D.A., Kinland, B.P., Gaylord, B. and Gaines, S.D. (2003) Lagrangian descriptions of marine larval dispersion. Marine Ecology Progress Series 260, 83–96.CrossRefGoogle Scholar
Simon, C.A., Ludford, A. and Wynne, S. (2006) Spionid polychaetes infesting cultured abalone, Haliotis midae, in South Africa. African Journal of Marine Science 28, 167–171.CrossRefGoogle Scholar
Taylor, E.B., Boughman, J.W., Groenenboom, M., Sniatynski, M., Schluter, D. and Gow, J.L. (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology 15, 343–355.CrossRefGoogle ScholarPubMed
Teske, P.R., Von der Heyden, S., McQuaid, C.D. and Barker, N.P. (2011) A review of marine phylogeography in southern Africa. South African Journal of Science 107, 43–53.CrossRefGoogle Scholar
Tournadre, J. (2014) Anthropogenic pressure on the open ocean: the growth of ship traffic revealed by altimeter data analysis. Geophysical Research Letters 41, 7924–7932.CrossRefGoogle Scholar
Viard, F., Ellien, C. and Dupont, L. (2006) Dispersal ability and invasion success of Crepidula fornicata in a single gulf: insights from genetic markers and larval-dispersal model. Helgoland Marine Research 60, 144–152.CrossRefGoogle Scholar
Von der Heyden, S. (2009) Why do we need to integrate population genetics into South African Marine Protected Area planning? African Journal of Marine Science 31, 263–269.CrossRefGoogle Scholar
Wares, J.P., Goldwater, D.S., Kong, B.Y. and Cunningham, C.W. (2002) Refuting a controversial case of a human-mediated marine species introduction. Ecology Letters 5, 577–584.CrossRefGoogle Scholar
Wares, J.P. and Pringle, J.M. (2008) Drift by drift: effective population size is limited by advection. BMC Evolutionary Biology 8, 235.CrossRefGoogle ScholarPubMed
White, C., Selkoe, K.A., Watson, J., Siegel, D.A., Zacherl, D.C. and Toonen, R.J. (2010) Ocean currents help explain population genetic structure. Proceedings of the Royal Society of London B. doi: 10.1098/rspb.2009.2214.Google ScholarPubMed
Williams, L., Matthee, C.A. and Simon, C.A. (2016) Dispersal and genetic structure of Boccardia polybranchia and Polydora hoplura (Annelida: Spionidae) in South Africa and their implications for aquaculture. Aquaculture 465, 235–244.CrossRefGoogle Scholar
Wolff, W.J. and Reise, K. (2002) Oyster imports as a vector for the introduction of alien species into northern and western European waters. In Leppakoski, E., Gollasch, S. and Olenin, S. (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Dordrecht: Kluwer, pp. 193–205.CrossRefGoogle Scholar
Woodin, S.A., Wethey, D.S. and Dubois, S.F. (2014) Population structure and spread of the polychaete Diopatra biscayensis along the French Atlantic coast: human-assisted transport by-passes larval dispersal. Marine Environmental Research 102, 110–121.CrossRefGoogle ScholarPubMed
Wrange, A.L., Charrier, G., Thonig, A., Alm Rosenblad, M., Blomberg, A., Havenhand, J.N., Jonsson, P.R. and Andre, C. (2016) The story of a hitchhiker: population genetic patterns in the invasive barnacle Balanus (Amphibalanus) improvisus Darwin 1854. PLoS ONE 11, e0147082.CrossRefGoogle ScholarPubMed
Wysor, B., Kooistra, W.H.C.F. and Fredericq, S. (2002) Comparative phylogeography of reticulate cladophoralean algae. Journal of Phycology 38, 38–39.Google Scholar