Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe

David Cordero; Marina Delgado; Baozhong Liu; Jennifer Ruesink; Carlos Saavedra

doi:10.1038/srep39745

journal article Open Access Jan 03, 2017

Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe

David Cordero Marina Delgado Baozhong Liu

Jennifer Ruesink Carlos Saavedra

Scientific Reports Vol. 7 No. 1 · Springer Science and Business Media LLC

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Abstract

AbstractGlobally, the Manila clam (Ruditapes philippinarum) stands as the second most important bivalve species in fisheries and aquaculture. Native to the Pacific coast of Asia, it is now well-established in North America and Europe, where its on-going management reflects local economic interests. The historic record of transfers spans the 20th century and suggests sequential movement from Japan to North America, as a hitch-hiker on oysters, and then intentional introduction in Europe, but global genetic data are missing. We have studied mitochondrial DNA and microsatellite markers in nine populations from Asia, North America and Europe. The results from the two types of markers indicated a good concordance of present-day genetic structure with the reported history of clam transfers across continents, and no evidence of relevant concealed introductions from continental Asia in Europe and North America. However, European populations showed a loss of genetic variability and significant genetic differentiation as compared to their American counterparts. Our study shows that in spite of the increasing ease for species to spread out of their native range, in the case of the Manila clam this has not resulted in new invasion waves in the two studied continents.

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References

88

[1]

Mack, R. N. et al. Issues in Ecology. Bull. Ecol. Soc. Am. 86, 249–250 (2005).

[2]

Rilov, G. & Crooks, J. A. Biological Invasions in Marine Ecosystems. Ecological, Management and Geographic Perspectives. (Springer-Verlag Berlin Heidelberg, 2009). 10.1007/978-3-540-79236-9

[3]

Utting, S. D. & Spencer, B. E. Introductions of marine bivalve molluscs into the United Kingdom for commercial culture- case histories. ICES Mar. Sci. Symp. 194, 84–91 (1992).

[4]

Savini, D. et al. The top 27 animal alien species introduced into Europe for aquaculture and related activities. J. Appl. Ichthyol. 26, 1–7 (2010). 10.1111/j.1439-0426.2010.01503.x

[5]

Mann, R. The role of introduced bivalve mollusc species in mariculture. In J. World Maricult. Soc. 14, 546–559 (1983). 10.1111/j.1749-7345.1983.tb00107.x

[6]

Handley, L. J. L., Manica, A., Goudet, J. & Balloux, F. Going the distance: human population genetics in a clinal world. Trends Genet. 23, 432–439 (2007). 10.1016/j.tig.2007.07.002

[7]

Dlugosch, K. M. & Parker, I. M. Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431–449 (2008). 10.1111/j.1365-294x.2007.03538.x

[8]

Ramachandran, S. et al. Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc. Natl. Acad. Sci. USA 102, 15942–15947 (2005). 10.1073/pnas.0507611102

[9]

Roman, J. & Darling, J. A. Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol. Evol. 22, 454–464 (2007). 10.1016/j.tree.2007.07.002

[10]

Geller, J. B., Darling, J. A. & Carlton, J. T. Genetic Perspectives on Marine Biological Invasions. Ann. Rev. Mar. Sci. 2, 367–393 (2010). 10.1146/annurev.marine.010908.163745

[11]

Uller, T. & Leimu, R. Founder events predict changes in genetic diversity during human-mediated range expansions. Glob. Chang. Biol. 17, 3478–3485 (2011). 10.1111/j.1365-2486.2011.02509.x

[12]

Hoos, P. M., Whitman Miller, A., Ruiz, G. M., Vrijenhoek, R. C. & Geller, J. B. Genetic and historical evidence disagree on likely sources of the Atlantic amethyst gem clam Gemma gemma (Totten, 1834) in California. Divers. Distrib. 16, 582–592 (2010). 10.1111/j.1472-4642.2010.00672.x

[13]

Fischer, M. L. et al. Historical invasion records can be misleading: Genetic evidence for multiple introductions of invasive raccoons (Procyon lotor) in Germany. PLoS One 10, 1–17 (2015).

[14]

Ponurovsky, S. K. & Yakovlev, Y. M. The reproductive biology of the Japanese littleneck, Tapes philippinarum. J. Shellfish Res. 11, 265–277 (1992).

[15]

Quayle, D. B. Distribution of introduced marine mollusca in British Columbia waters. J. Fish. Res. Board Canada 21, 1155–1181 (1964). 10.1139/f64-102

[16]

Cohen, A. N. & Carlton, J. T. Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta. Report, US Fish and Wildlife Service (1995).

[17]

Flassch, J. & Leborgne, Y. Introduction in Europe, from 1972 to 1980, of the Japanese Manila clam. ICES mar. Sci. Symp 194, 92–96 (1992).

[18]

Breber, P. L’introduzione e l’allevamento in Italia dell’Arsella del Pacifico, Tapes semidecussatus Reeve (Bivalvia: Veneridae). Oebalia 9, 675–680 (1985).

[19]

Hopkins, C. Actual and potential effects of introduced marine organisms in Norwegian waters, including Svalbard. Directorate for Nature Management (Norway) (2001). 10.1007/978-94-015-9956-6_26

[20]

A history of invasion: COI phylogeny of Manila clam Ruditapes philippinarum in Europe

Stefania Chiesa, Livia Lucentini, Rosa Freitas et al.

Fisheries Research 2017 10.1016/j.fishres.2016.07.024

[21]

Albayrak, S., Aslan, H. & Balkis, H. A contribution to the Aegean Sea fauna: Ruditapes philippinarum (Adams & Reeve, 1850) [Bivalvia: Veneridae]. Isr. J. Zool. 47, 299–300 (2001).

[22]

Jensen, A. C., Humphreys, J. & Grisley, C. Naturalization of the Manila clam (Tapes philippinarum), an alien species, and establishment of a clam fishery within Poole Harbour, Dorset. J. Mar. Biol. Ass. U. K. 84, 1069–1073 (2004). 10.1017/s0025315404010446h

[23]

Breber, P. In Invasive Aquatic species of Europe (eds. Leppäkoski, E., Gollasch, S. & Olenin, S. ) 120–126 (Kluwer, 2002). 10.1007/978-94-015-9956-6_13

[24]

Walne, P. R. Culture of Bivalve molluscs. (John wiley and Sons, 1970).

[25]

Jones, G. G., Sanford, C. L. & Jones, B. L. Manila Clams : Hatchery and Nursery Methods. Innovative Aquaculture Products Ltd. (Innovative Aquaculture Products Ltd., 1993).

[26]

Auby, I. Evolution of the Biologic Richness in the Arcachon Basin. Report. Ifremer/Société Scientifique d’Arcachon (1993).

[27]

Bendell, L. I. Evidence for declines in the native Leukoma staminea as a result of the intentional introduction of the non-native Venerupis philippinarum in coastal British Columbia, Canada. Estuaries and Coasts 1–12, doi: 10.1007/s12237-013-9677-1 (2013). 10.1007/s12237-013-9677-1

[28]

Juanes, J. A. et al. Differential distribution pattern of native Ruditapes decussatus and introduced Ruditapes phillippinarum clam populations in the Bay of Santander (Gulf of Biscay): Considerations for fisheries management. Ocean Coast. Manag. 69, 316–326 (2012). 10.1016/j.ocecoaman.2012.08.007

[29]

Bidegain, G. & Juanes, J. A. Does expansion of the introduced Manila clam Ruditapes philippinarum cause competitive displacement of the European native clam Ruditapes decussatus? J. Exp. Mar. Bio. Ecol. 445, 44–52 (2013). 10.1016/j.jembe.2013.04.005

[30]

Hurtado, N. S., Pérez-García, C., Morán, P. & Pasantes, J. J. Genetic and cytological evidence of hybridization between native Ruditapes decussatus and introduced Ruditapes philippinarum (Mollusca, Bivalvia, Veneridae) in NW Spain. Aquaculture 311, 123–128 (2011). 10.1016/j.aquaculture.2010.12.015

[31]

Habtemariam, B. T., Arias, A., García-Vázquez, E. & Borrell, Y. J. Impacts of supplementation aquaculture on the genetic diversity of wild Ruditapes decussatus from northern Spain. Aquac. Environ. Interact. 6, 241–254 (2015). 10.3354/aei00128

[32]

Kitada, S. et al. Molecular and morphological evidence of hybridization between native Ruditapes philippinarum and the introduced Ruditapes form in Japan. Conserv. Genet. 14, 717–733 (2013). 10.1007/s10592-013-0467-x

[33]

Sekine, Y., Yamakawa, Y., Takazawa, S., Yingping, L. & Toba, M. Geographic variation in the COXI gene of the Short-neck clam Ruditapes philippinarum in coastal regions of Japan and china. Venus 65, 229–224 (2006).

[34]

Vargas, K. et al. Allozyme variation of littleneck clam Ruditapes philippinarum and genetic mixture analysis of foreign clams in Ariake Sea and Shiranui Sea off Kyushu Island, Japan. Fish. Sci. 74, 533–543 (2008). 10.1111/j.1444-2906.2008.01556.x

[35]

Liu, X. et al. AFLP analysis revealed differences in genetic diversity of four natural populations of Manila clam (Ruditapes philippinarum) in China. Acta Oceanol. Sin. 26, 150–158 (2007).

[36]

Mao, Y., Gao, T., Yanagimoto, T. & Xiao, Y. Molecular phylogeography of Ruditapes philippinarum in the Northwestern Pacific Ocean based on COI gene. J. Exp. Mar. Bio. Ecol. 407, 171–181 (2011). 10.1016/j.jembe.2011.06.002

[37]

An, H. S., Park, K. J., Cho, K. C., Han, H. S. & Myeong, J. I. Genetic structure of Korean populations of the clam Ruditapes philippinarum inferred from microsatellite marker analysis. Biochem. Syst. Ecol. 44, 186–195 (2012). 10.1016/j.bse.2012.05.007

[38]

Xing, K., Gao, M. L. & Li, H. J. Genetic differentiation between natural and hatchery populations of Manila clam (Ruditapes philippinarum) based on microsatellite markers. Genet. Mol. Res. 13, 237–45 (2014). 10.4238/2014.january.17.7

[39]

Cigarrı́a, J. & Fernández, J. M. Management of Manila clam beds. Aquaculture 182, 173–182 (2000). 10.1016/s0044-8486(99)00257-4

[40]

Bald, J. et al. A system dynamics model for the management of the Manila clam, Ruditapes philippinarum (Adams and Reeve, 1850) in the Bay of Arcachon (France). Ecol. Modell. 220, 2828–2837 (2009). 10.1016/j.ecolmodel.2009.03.031

[41]

Choi, Y. et al. The study of stock assessment and management implications of the Manila clam, Ruditapes philippinarum in Taehwa river of Ulsan. 27, 107–114 (2011).

[42]

Chiesa, S. et al. The invasive Manila clam Ruditapes philippinarum (Adams and Reeve, 1850) in Northern Adriatic Sea: Population genetics assessed by an integrated molecular approach. Fish. Res. 110, 259–267 (2011). 10.1016/j.fishres.2011.04.013

[43]

Mura, L. et al. Genetic variability in the Sardinian population of the manila clam, Ruditapes philippinarum . Biochem. Syst. Ecol. 41, 74–82 (2012). 10.1016/j.bse.2011.11.002

[44]

Steele, E. N. The inmigrant oyster. (Pacific Oyster Growers Association, 1964).

[45]

Hedgecock, D., Chow, V. & Waples, R. S. Effective population numbers of shellfish brood stocks estimated from temporal variances in allelic frequencies. Aquaculture 108, 215–232 (1992). 10.1016/0044-8486(92)90108-w

[46]

Borrell, Y. J. et al. Microsatellites and multiplex PCRs for assessing aquaculture practices of the grooved carpet shell Ruditapes decussatus in spain. Aquaculture 426–427, 49–59 (2014). 10.1016/j.aquaculture.2014.01.010

[47]

Ni, G., Li, Q., Kong, L. & Yu, H. Comparative phylogeography in marginal seas of the northwestern Pacific. Mol. Ecol. 23, 534–548 (2014). 10.1111/mec.12620

[48]

Excoffier, L. & Lischer, H. E. L. 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 (2010). 10.1111/j.1755-0998.2010.02847.x

[49]

Tamura, K., Nei, M. & Kumar, S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101, 11030–5 (2004). 10.1073/pnas.0404206101

[50]

Inference of Population Structure Using Multilocus Genotype Data

Jonathan K Pritchard, Matthew Stephens, Peter Donnelly

Genetics 2000 10.1093/genetics/155.2.945

Showing 50 of 88 references

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Published: Jan 03, 2017
Vol/Issue: 7(1)
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Cite This Article

David Cordero, Marina Delgado, Baozhong Liu, et al. (2017). Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe. Scientific Reports, 7(1). https://doi.org/10.1038/srep39745

Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe

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