Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-18T20:21:30.073Z Has data issue: false hasContentIssue false

Meso-scale genetic structure of the intertidal, crevice-dwelling, stalked barnacle Ibla cumingi (Crustacea: Cirripedia): an interplay of life history and local hydrographic conditions

Published online by Cambridge University Press:  13 July 2010

Priscilla T.Y. Leung*
Affiliation:
The Swire Institute of Marine Science, The University of Hong Kong, Hong Kong, China Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong, China
Brian Morton
Affiliation:
The Swire Institute of Marine Science, The University of Hong Kong, Hong Kong, China
W.C. Ng
Affiliation:
The Swire Institute of Marine Science, The University of Hong Kong, Hong Kong, China Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong, China
*
Correspondence should be addressed to: P.T.Y. Leung, The Swire Institute of Marine Science and Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Hong Kong, China email: [email protected]

Abstract

Variation in life history characteristics is believed to play an important role in dispersal and thus shaping the population and genetic structure of marine invertebrates. The genetic structure of Ibla cumingi, a small intertidal stalked barnacle that broods lecithotrophic larvae, was evaluated using 145 random amplified polymorphic DNA markers on 100 individuals from five locations across Hong Kong waters. Shallow genetic structure was observed along open-coast shores, and there was no indication of isolation by geographical distance. A significant genetic divergence, however, was observed between samples inside and outside Tolo Harbour, a semi-enclosed, sheltered and estuarine bay located in the north-eastern quadrant of Hong Kong, indicating the presence of a genetic sub-structuring pattern. In addition, relatively lower genetic diversities were described for samples inside Tolo Harbour than those from open-coast shores. This could be associated with an increase in inbreeding events attributed to local settlement caused by larval retention. This study provides an insight into how the interaction of life history and local, enclosed, hydrographic conditions could result in a substantial genetic structuring of I. cumingi over a meso-scale geographical distance.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allison, G.W., Gaines, S.D., Lubchenco, J. and Possingham, H.P. (2003) Ensuring persistence of marine reserves: catastrophes require adopting an insurance factor. Ecological Applications 13, S8S24.Google Scholar
Anderson, D.T. (1994) Barnacles: structure, function, development and evolution. London: Chapman & Hall.Google Scholar
Ayers, K.L. and Waters, J.M. (2005) Marine biogeographic disjuction in central New Zealand. Marine Biology 147, 10451052.CrossRefGoogle Scholar
Bilton, D.T., Paula, J. and Bishop, J.D.D. (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science 55, 937952.CrossRefGoogle Scholar
Bohonak, A.J. (1999) Dispersal, gene flow, and population structure. Quarterly Review of Biology 74, 2145.Google Scholar
Borsa, P., Blanquer, A. and Berrebi, P. (1997) Genetic structure of the flounders Platichthys flesus and P. stellatus at different geographic scales. Marine Biology 129, 233246.Google Scholar
Botsford, L.W., Micheli, F. and Hastings, A. (2003) Principles for the design of marine reserves. Ecological Applications 13, S25S31.CrossRefGoogle Scholar
Britton, J.C. (1990) The intertidal crevice fauna of Tolo Channel and Harbour, New Territories, Hong Kong. In Morton, B. (ed.) The marine flora and fauna of Hong Kong and Southern China, Hong Kong. Proceedings of the Second International Marine Biological Workshop: the marine flora and fauna of Hong Kong and Southern China, Hong Kong 1986. Hong Kong: Hong Kong University Press, pp. 803835.Google Scholar
Buonaccorsi, V.P., Kimbrell, C.A., Lynn, E.A. and Vetter, R.D. (2005) Limited realized dispersal and introgressive hybridization influence genetic structure and conservation strategies for brown rockfish, Sebastes auriculatus. Conservation Genetics 6, 697713.Google Scholar
Chan, B.K.K., Morritt, D. and Williams, G.A. (2001) Effect of salinity and recruitment on the distribution of Tetraclita squamosa and Tetraclita japonica (Cirripedia; Balanomorpha) in Hong Kong. Marine Biology 138, 9991009.Google Scholar
Cheung, M.K., Chu, K.H., Li, C.P., Kwan, H.S. and Wong, C.K. (2008) Genetic diversity of picoeukaryotes in a semi-enclosed harbour in the subtropical western Pacific Ocean. Aquatic Microbial Ecology 53, 295305.Google Scholar
Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 26112620.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google Scholar
Falush, D., Stephens, M. and Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 15671587.Google Scholar
Foster, B.A. (1987) Barnacle ecology and adaptation. In Southward, A.J. (ed.) Crustacean Issues 5: Barnacle Biology. Rotterdam: A.A. Balkema, pp. 113133.Google Scholar
Ganmanee, M., Narita, T. and Sekiguchi, H. (2004) Long-term investigation of spatio-temporal variations in faunal composition and species richness of megabenthos in Ise Bay, central Japan. Journal of Oceanography 60, 10711083.Google Scholar
Goldson, A.J., Hughes, R.N. and Gliddon, C.J. (2001) Population genetic consequences of larval dispersal mode and hydrography: a case study with bryozoans. Marine Biology 138, 10371042.Google Scholar
Grosberg, R.K. (1987) Limited dispersal and proximty-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41, 372384.Google Scholar
Guo, S.W. and Thompson, E.A. (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361372.CrossRefGoogle ScholarPubMed
Hedgecock, D. (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bulletin of Marine Science 39, 550565.Google Scholar
Hedgecock, D., Launey, S., Pudovkin, A.I., Naciri, Y., Lapègue, S. and Bonhomme, F. (2007) Small effective number of parents (N b) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Marine Biology 150, 11731182.Google Scholar
Hellberg, M.E., Burton, R.S., Neigel, J.E. and Palumbi, S.R. (2002) Genetic assessment of connectivity among marine populations. Bulletin of Marine Science S70, 273290.Google Scholar
Høeg, J.T., Achituv, Y., Chan, B.K.K., Chan, K., Jensen, P.G. and Perez-Losada, M. (2009) Cypris morphology in the barnacles Ibla and Paralepas (Crustacea: Cirripedia: Thoracica): implications for cirripede evolution. Journal of Morphology 270, 241255.CrossRefGoogle ScholarPubMed
Hoelzel, A.R. and Green, A. (1992) Analysis of population-level variation by sequencing PCR-amplified DNA. In Hoelzel, A.R. (ed.) Molecular genetic analysis of populations: a practical approach. Oxford: Oxford University Press, pp. 159186.Google Scholar
Ignacio, B.L., Absher, T.M., Lazoski, C. and Sole-Cava, A.M. (2000) Genetic evidence of the presence of two species of Crassostrea (Bivalvia: Ostreidae) on the coast of Brazil. Marine Biology 136, 987991.Google Scholar
Johnson, M.S. and Black, R. (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Marine Biology 70, 157164.CrossRefGoogle Scholar
Johnson, M.S. and Black, R. (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38, 13711383.Google Scholar
Jones, D.S., Hewitt, M.A. and Sampey, A. (2000) A checklist of the Cirripedia of the South China Sea. Raffles Bulletin of Zoology S8, 233307.Google Scholar
Kirkendale, L.A. and Meyer, C.P. (2004) Phylogeography of the Patelloida profunda group (Gastropoda: Lottidae): diversification in a dispersal-driven marine system. Molecular Ecology 13, 27492762.Google Scholar
Kordos, L.M. and Burton, R.S. (1993) Genetic differentiation of Texas Gulf Coast populations of the blue crab Callinectes sapidus. Marine Biology 117, 227233.CrossRefGoogle Scholar
Lee, J.H.W., Huang, Y., Dickman, M. and Jayawardena, A.W. (2003) Neural network modeling of coastal algal blooms. Ecological Modelling 159, 179201.Google Scholar
Lessios, H.A., Kane, J. and Robertson, D.R. (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57, 20262036.Google Scholar
Leung, T.Y. (2003) The ecology and reproductive biology of two intertidal barnacles, Capitulum mitella and Ibla cumingi (Cirripedia: Pedunculata), in Hong Kong. PhD thesis. The University of Hong Kong, Hong Kong.Google Scholar
Liu, R. and Ren, X. (1985) Studies on Chinese Cirripedia (Crustacea) VI: Suborder Lepadomorpha. Studia Marina Sinica 25, 179281.Google Scholar
Lui, K.K.Y. (2005) Ecology of commercially important stomatopods in Hong Kong. MPhil thesis. The University of Hong Kong, Hong Kong.Google Scholar
Lui, K.K.Y., Leung, P.T.Y., Ng, W.C. and Leung, K.M.Y. (2010) Genetic variation of Oratosquilla oratoria (Crustacea: Stomatopoda) across Hong Kong waters elucidated by mitochondrial DNA control region sequences. Journal of the Marine Biological Association of the United Kingdom 90, 623631.CrossRefGoogle Scholar
Lynch, M. and Milligan, B.G. (1994) Analysis of population genetic structure with RAPD markers. Molecular Ecology 3, 9199.CrossRefGoogle ScholarPubMed
McCormack, G.P., Powell, R. and Keegan, B.F. (2000) Comparative analysis of two populations of the brittle star Amphiura filiformis (Echinodermata: Ophiuroidea) with different life history strategies using RAPD markers. Marine Biotechnology 2, 100106.Google Scholar
Miller, K.J. (1998) Short-distance dispersal of black coral larvae: inference from spatial analysis of colony genotypes. Marine Ecology Progress Series 163, 225233.CrossRefGoogle Scholar
Morton, B. (1982) An introduction to Hong Kong's marine environment with special reference to the north-eastern New Territories. In Morton, B. and Tseng, C.K. (eds) Proceedings of the First International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and southern China. Hong Kong: Hong Kong University Press, pp. 2554.CrossRefGoogle Scholar
Morton, B. and Harper, E. (1995) An introduction to the Cape d'Aguilar Marine Reserve, Hong Kong. Hong Kong: Hong Kong University Press.Google Scholar
Morton, B. and Morton, J. (1983) The sea shore ecology of Hong Kong. Hong Kong: Hong Kong University Press.Google Scholar
Nei, M. (1972) Genetic distance between populations. American Naturalist 106, 283292.Google Scholar
Nei, M. (1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 70, 33213323.Google Scholar
Ng, W.C., Leung, F.C.C., Chak, S.T.C., Slingsby, G. and Williams, G.A. (2010) Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores. Marine Biology 157, 325337.Google Scholar
Ng, W.C. and Morton, B. (2003) Genetic structure of the scleractinian coral Platygyra sinensis in Hong Kong. Marine Biology 143, 963968.CrossRefGoogle Scholar
O'Foighil, D., Marshall, B.A., Hilbish, T.J. and Pino, M.A. (1999) Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biological Bulletin. Marine Biological Laboratory, Woods Hole 196, 122126.Google Scholar
Palmer, A.R. and Strathmann, R.R. (1981) Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia 48, 308318.Google Scholar
Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics 25, 547572.Google Scholar
Palumbi, S.R. (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, S146S158.Google Scholar
Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.Google Scholar
Quinteiro, J., Rodriguez-Castro, J. and Rey-Mendez, M. (2007) Population genetic structure of the stalked barnacle Pollicipes pollicipes (Gmelin, 1789) in the northeastern Atlantic: influence of coastal currents and mesoscale hydrographic structures. Marine Biology 153, 4760.Google Scholar
Rocha, L.A., Robertson, D.R., Roman, J. and Bowen, B.W. (2005) Ecological speciation in tropical reef fishes. Proceedings of the Royal Society B—Biological Sciences 272, 573579.Google Scholar
Sköld, M., Wing, S.R. and Mladenov, V. (2003) Genetic subdivision of sea star with high dispersal capability in relation to physical barriers in a fjordic seascape. Marine Ecology Progress Series 250, 163174.CrossRefGoogle Scholar
Taylor, M.S. and Hellberg, M.E. (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299, 107109.Google Scholar
Teske, P.R., Papadopoulos, I., Zardi, G.I., McQuaid, C.D., Edkins, M.T., Griffths, C.L. and Barker, N.P. (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Marine Biology 152, 697711.CrossRefGoogle Scholar
Todd, C.D., Lambert, W.J. and Thorpe, J.P. (1998) The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae ‘for’ dispersal? Journal of Experimental Marine Biology and Ecology 228, 128.Google Scholar
Vekemans, X. (2002) AFLP-SURV, Version 1.0. Laboratoire de Génétique et Ecologie Végétale, Belgium: Université Libre de Bruxelles.Google Scholar
Watts, R.J. and Johnson, M.S. (2004) Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Marine and Freshwater Research 55, 641651.Google Scholar
Watts, R.J., Johnson, M.S. and Black, R. (1990) Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in Western Australia. Marine Biology 105, 145151.Google Scholar
Wilson, A.B., Boates, J.S. and Snyder, M. (1997) Genetic isolation of populations of the gammaridean amphipod, Corophium volutator, in the Bay of Fundy, Canada. Molecular Ecology 6, 917923.Google Scholar
Wu, R.S.S. (1982) Period defaunation and recovery in a sub-tropical epibenthic community in relation to organic pollution. Journal of Experimental Marine Biology and Ecology 64, 253269.Google Scholar
Yan, Y., Chan, B.K.K. and Williams, G.A. (2006) Reproductive development of the barnacle Chthamalus malayensis in Hong Kong: implications for the life-history patterns of barnacles on seasonal, tropical shores. Marine Biology 148, 875887.Google Scholar
Yan, Y., Haoru, C., Huang, L.M. and Sun, L.H. (2005) Larval development of the barnacle Ibla cumingi (Cirripedia: Pedunculata: Iblidae) reared in the laboratory. Journal of the Marine Biological Association of the United Kingdom 85, 903907.Google Scholar