Abstract
Understanding patterns of dispersal of marine organisms among estuaries is important for the conservation of biodiversity and the design of marine park networks. Whereas numerous studies have recently assessed dispersal potential among key marine vertebrates and habitat-forming macroalgae, relatively few have assessed the potential for dispersal in ecologically important benthic polychaete worms. Here, we used phylogeographic analyses to test for evidence of genetic disjunctions among populations of polychaete worms from different estuaries in southeastern Australia. Our study focused on two species from the family Nephtyidae (Aglaophamus australiensis and Nephtys longipes) that are found intertidally in soft sediments in estuaries. Both species have planktonic larvae, but little is known about the survival times of the larvae, or their potential to disperse to other estuaries rather than settling locally. Genetic analyses of two mitochondrial (cytochrome c oxidase subunit I and 16S rDNA) markers in both species and a nuclear marker (28S rDNA) in A. australiensis were carried out to assess whether geographically distinct populations show genetic differences. Little evidence of genetic differentiation among populations was found, despite a high level of genetic diversity within each species. Although some significant population pairwise FST differences were detected for both species via AMOVA, these appeared largely driven by singleton haplotype diversity, whereas several common haplotypes were shared among all populations. Our results suggest that sedentary, benthic estuarine organisms with planktonic larvae can disperse to distant estuaries with the aid of tidal flushing and coastal ocean currents.
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References
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2010) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193. doi:10.1890/10-1510.1
Barroso R, Klautau M, Solé-Cava AM, Paiva PC (2010) Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Mar Biol 157:69–80. doi:10.1007/s00227-009-1296-9
Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho G (ed) Advances in Molecular Ecology., NATO-ASI workshop seriesIOS Press, Amsterdam, pp 39–53
Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568
Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952. doi:10.1006/ecss.2002.1037
Borda E, Kudenov JD, Chevaldonné P, Blake JA, Desbruyères D, Fabri M-C, Hourdez S, Pleijel F, Shank TM, Wilson NG, Schulze A, Rouse GW (2013) Cryptic species of Archinome (Annelida: Amphinomida) from vents and seeps. Proc R Soc Lond B Biol Sci. doi:10.1098/rspb.2013.1876
Bors EK, Rowden AA, Maas EW, Clark MR, Shank TM (2012) Patterns of deep-sea genetic connectivity in the New Zealand region: implications for management of benthic ecosystems. PLoS One 7:e49474. doi:10.1371/journal.pone.0049474
Bradbury IR, Campana SE, Bentzen P (2008a) Low genetic connectivity in an estuarine fish with pelagic larvae. Can J Fish Aquat Sci 65:147–158. doi:10.1139/f07-154
Bradbury IR, Laurel B, Snelgrove PVR, Bentzen P, Campana SE (2008b) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc R Soc Biol Sci Ser B 275:1803–1809. doi:10.1098/rspb.2008.0216
Brown CW (1990) The significance of the South Atlantic Equatorial countercurrent to the ecology of the green turtle breeding population of Ascension Island. J Herpetol 24:81–84. doi:10.2307/1564294
Caron A, Boucher L, Desrosiers G, Retiere C (1995) Population dynamics of the polychaete Nephtys caeca in an intertidal estuarine environment. J Mar Biol Assoc UK 75:871–884. doi:10.1017/S0025315400038212 (Quebec, Canada)
Carr CM, Hardy SM, Brown TM, Macdonald TA, Hebert PDN (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One 6:e22232. doi:10.1371/journal.pone.0022232
Chust G, Albaina A, Aranburu A, Borja Á, Diekmann OE, Estonba A, Franco J, Garmendia JM, Iriondo M, Muxika I, Rendo F, Rodríguez JG, Ruiz-Larrañaga O, Serrão EA, Valle M (2013) Connectivity, neutral theories and the assessment of species vulnerability to global change in temperate estuaries. Estuar Coast Shelf Sci 131:52–63. doi:10.1016/j.ecss.2013.08.005
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x
Coleman MA (2013) Connectivity of the habitat-forming kelp, Ecklonia radiata within and among estuaries and open coast. PLoS One 8:e64667. doi:10.1371/journal.pone.0064667
Coleman MA, Chambers J, Knott NA, Malcolm HA, Harasti D, Jordan A, Kelaher BP (2011) Connectivity within and among a network of temperate marine reserves. PLoS One 6:e20168. doi:10.1371/journal.pone.0020168
Coleman MA, Feng M, Roughan M, Cetina-Heredia P, Connell SD (2013) Temperate shelf water dispersal by Australian boundary currents: implications for population connectivity. Limnol Oceanogr Fluids Environ 3:295–309. doi:10.1215/21573689-2409306
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466. doi:10.1146/annurev.marine.010908.163757
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527. doi:10.1126/science.1122039
Dixon-Bridges K, Gladstone W, Hutchings P (2014) Two new species of Micronephthys Friedrich, 1939 and one new species of Nephtys Cuvier, 1817 (Polychaeta: Phyllodocida: Nephtyidae) from eastern Australia with notes on Aglaophamus australiensis (Fauchald, 1965) and a key to all Australian species. Zootaxa 3872:513–540. doi:10.11646/zootaxa.3872.5.5
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299
Glasby CJ, Wei N-WV, Gibb KS (2013) Cryptic species of Nereididae (Annelida: Polychaeta) on Australian coral reefs. Invertebr Syst 27:245–264. doi:10.1071/IS12031
Hutchings P (1992) Ballast water introductions of exotic marine organisms into Australia: current status and management options. Mar Pollut Bull 25:196–199. doi:10.1016/0025-326X(92)90225-U
Hutchings P (2004) Polychaetes — their biological diversity. Rec S Aust Mus 7:39–49 (Adel)
Jenkins KM, Kingsford RT, Closs GP, Wolfenden BJ, Matthaei CD, Hay SE (2011) Climate change and freshwater ecosystems in Oceania: an assessment of vulnerability and adaptation opportunities. Pac Conserv Biol 17:201–219
Johannesson K (1988) The paradox of Rockall—why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513
Jolly MT, Jollivet D, Gentil F, Thiebaut E, Viard F (2004) Sharp genetic break between Atlantic and English channel populations of the polychaete Pectinaria koreni, along the North coast of France. Heredity 94:23–32. doi:10.1038/sj.hdy.6800543
Jolly MT, Viard F, Gentil F, Thiebaut E, Jollivet D (2006) Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Mol Ecol 15:1841–1855. doi:10.1111/j.1365-294X.2006.02910.x
Kennish MJ (2002) Environmental threats and environmental future of estuaries. Environ Conserv 29:78–107. doi:10.1017/S0376892902000061
Kesäniemi JE, Geuverink E, Knott KE (2012) Polymorphism in developmental mode and its effect on population genetic structure of a spionid polychaete, Pygospio elegans. Integ Comp Biol 52:181–196. doi:10.1093/icb/ics064
Meissner K, Bick A, Guggolz T, Götting M (2014) Spionidae (Polychaeta: Canalipalpata: Spionida) from seamounts in the NE Atlantic. Zootaxa 3786:201–245. doi:10.11646/zootaxa.3786.3.1
Nygren A, Pleijel F (2011) From one to ten in a single stroke—resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex. Mol Phylogenet Evol 58:132–141. doi:10.1016/j.ympev.2010.10.010
Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology, University of Hawaii, Honolulu
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460
Piggott MP, Banks SC, Tung P, Beheregaray LB (2008) Genetic evidence for different scales of connectivity in a marine mollusc. Mar Ecol Prog Ser 365:127–136. doi:10.3354/Meps07478
Roughan M, Middleton JH (2004) On the East Australian current: variability, encroachment, and upwelling. J Geophys Res Ocean 109:C07003. doi:10.1029/2003JC001833
Roy PS, Williams RJ, Jones AR, Yassini I, Gibbs PJ, Coates B, West RJ, Scanes PR, Hudson JP, Nichol S (2001) Structure and function of south-east Australian estuaries. Estuar Coast Shelf Sci 53:351–384. doi:10.1006/ecss.2001.0796
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632. doi:10.1093/icb/37.6.621
Schüller M, Hutchings PA (2012) New species of Terebellides (Polychaeta: Trichobranchidae) indicate long-distance dispersal between western South Atlantic deep-sea basins. Zootaxa: 1–31
Sherman CDH, Hunt A, Ayre DJ (2008) Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol J Linn Soc 95:106–116. doi:10.1111/j.1095-8312.2008.01044.x
Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Front Zool 4:6. doi:10.1186/1742-9994-4-6
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121
Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTech 10:506–513
Acknowledgments
We thank C. McGrath and J. Tan for laboratory assistance, and J. Pierson for assistance with some analyses. P. Rodgers, A. Murray and S. Keable helped with collecting, and S. Lindsey with photography. Funding was provided by the Australian Museum and by research funds for CIF from the Fenner School of Environment and Society at the Australian National University.
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Communicated by C. Riginos.
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Smith, L.M., Hutchings, P. & Fraser, C.I. Molecular evidence supports coastal dispersal among estuaries for two benthic marine worm (Nephtyidae) species in southeastern Australia. Mar Biol 162, 1319–1327 (2015). https://doi.org/10.1007/s00227-015-2671-3
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DOI: https://doi.org/10.1007/s00227-015-2671-3