Hostname: page-component-7479d7b7d-8zxtt Total loading time: 0 Render date: 2024-07-13T15:38:02.877Z Has data issue: false hasContentIssue false
  • English
  • Français

When anthropogenic translocation meets cryptic speciation globalized bouillon originates; molecular variability of the cosmopolitan freshwater cyclopoid Macrocyclops albidus (Crustacea: Copepoda)

Published online by Cambridge University Press:  14 March 2012

T. Karanovic  and
M. Krajicek
T. Karanovic*
Affiliation:
Department of Life Sciences, Hanyang University, Seoul 133-791, South Korea IMAS, University of Tasmania, Hobart TAS 7001, Australia
M. Krajicek
Affiliation:
Department of Ecology, Charles University in Prague, Vinicna 7, 12844 Prague 2, Czech Republic
*
*Corresponding author: tomislav.karanovic@utas.edu.au
Get access

Abstract

Invasive species are a global problem, which costs the world economy billions of dollars and world ecosystems millions of tons of herbicides, pesticides and other cides. Anthropogenic translocation of freshwater copepods associated with early shipping activities was postulated for some time, but was never tested with molecular tools. Here, we examine global molecular diversity of one cyclopoid species, test if the current cosmopolitan distribution is a result of anthropogenic translocation or natural dispersal, and investigate a possibility of cryptic speciation. We use patterns of haplotype frequency of DNA and RNA sequences of four genes (12S, 16S, 18S and cytB) and 11 populations (from England, Scotland, France, Germany, USA, New Zealand and Australia) to test inter- and intrapopulation variability, and three different methods (neighbour joining (NJ), maximum likelihood (ML) and maximum parsimony (MP)) for reconstructing their phylogenetic relationships. They were then tested against two competing hypotheses, and complemented by comparative morphology of microcharacters. Reconstructed phylogenies present strong evidence for anthropogenic translocation, with the same haplotype found in highly disjunct populations in Western Australia, Germany and the USA. Four different clades were revealed with the 12S, 16S and cytB genes, probably representing four cryptic species. Morphological examination of females of two clades contributed a set of microcharacters that can be used in the future taxonomic revision of this species complex. We prove for the first time that cuticular pores and sensilla are homologous structures. This research provides evidence for both homogenization of world freshwater fauna and our inadequate methods of identifying some of its most common species.

Keywords

Invasive speciesecosystem degradationfreshwaterglobalized faunahaplotype frequency
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 48 , Issue 1 , 2012 , pp. 63 - 80
Copyright
© EDP Sciences, 2012

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

Abbott, R.J., James, J.K., Milne, R.I. and Gillies, A.C.M., 2003. Plant introduction, hybridization and gene flow. Philos. Trans. R. Soc. Lond., Ser. A, 358, 1123–1132.CrossRefGoogle Scholar
Alekseev, V., Dumont, H.J., Pensaert, J., Baribwegure, D. and Vanfleteren, J.R., 2005. A redescription of Eucyclops serrulatus (Fischer, 1851) (Crustacea: Copepoda: Cyclopoida) and some related taxa, with a phylogeny of the E. serrulatus-group. Zool. Scr., 35, 123–147.CrossRefGoogle Scholar
Audzijonyte, A., Damgaard, J., Varvio, S.-L., Vainio, J.K. and Väinölä, R., 2005. Phylogeny of Mysis (Crustacea, Mysida): history of continental invasions inferred from molecular and morphological data. Cladistics, 21, 575–596.CrossRefGoogle Scholar
Braga, E., Zardoya, R., Meyer, A. and Yen, J., 1999. Molecular and nuclear rRNA based copepod phylogeny with emphasis on the Euchaetidae (Calanoida). Mar. Biol., 133, 79–90.CrossRefGoogle Scholar
Bulnheim, H.P., 1985. Genetic differentiation between natural populations of Gammarus tigrinus (Crustacea, Amphipoda) with reference to its range extension in European continental waters. Arch. Hydrobiol., 102, 273–290.Google Scholar
De Filippis, V.R. and Moore, W.S., 2000. Resolution of phylogenetic relationships among recently evolved species as a function of amount of DNA sequence: an empirical study based on woodpeckers (Aves: Picidae). Mol. Phyl. Evol., 16, 143–160.CrossRefGoogle Scholar
Dunstan, P.K. and Johnson, C.R., 2007. Mechanisms of invasions: can the recipient community influence invasion rates? Bot. Mar., 50, 361–372.CrossRefGoogle Scholar
Dussart, B. and Defaye, D., 2006. World Directory of Crustacea Copepoda of Inland Waters, II – Cyclopiformes, Backhuys Publishers, Leiden, 354 p.Google Scholar
Feldman, C.R. and Omland, K.E., 2004. Phylogenetics of the common raven complex (Corvus: Corvidae) and the utility of ND4, COI and intron 7 of the β-fibrinogen gene in avian molecular systematic. Zool. Scri., 34, 145–156.CrossRefGoogle Scholar
Gregg, M., Rigby, G. and Hallegraeff, G.M., 2009. Review of two decades of progress in the development of management options for reducing or eradicating phytoplankton, zooplankton and bacteria in ship's ballast water. Aquat. Invas., 4, 521–565.CrossRefGoogle Scholar
Grey, D.K., Johengen, T.H., Reid, D.F. and MacIsaac, H.J., 2007. Efficacy of open-ocean ballast water exchange as a means of preventing invertebrate invasions between freshwater ports. Limnol. Oceanogr., 52, 2386–2397.CrossRefGoogle Scholar
Grigorovich, I.A., Colautti, R.I., Mills, E.L., Holeck, K., Ballert, A.G. and MacIsaac, H.J., 2003. Ballast-mediated animal introduction in the Laurentian Great Lakes: retrospective and prospective analyses. Can. J. Fish. Aquat. Sci., 60, 740–756.CrossRefGoogle Scholar
Guindon, S. and Gascuel, O., 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst. Biol., 52, 696–704.CrossRefGoogle ScholarPubMed
Hasegawa, M., Kishino, H. and Yano, T., 1985. Dating of the human ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol., 22, 160–174.CrossRefGoogle ScholarPubMed
Havel, J.E., Lee, C.E. and Vander Zanden, M.J., 2005. Do reservoirs facilitate invasions into landscapes? BioScience, 55, 518–525.CrossRefGoogle Scholar
Hewitt, C.L., Campbell, M.L. and Schaffelke, B., 2007. Introductions of seaweeds: accidental transfer pathways and mechanisms. Bot. Mar., 50, 326–337.CrossRefGoogle Scholar
Hood, J., 2003. Marked for Misfortune: An Epic Tale of Shipwreck, Human Endeavour and Survival in the Age of Sail, Conway Maritime Press, London, 288 p.Google Scholar
Horvath, T.G., Whitman, R.L. and Last, L.L., 2001. Establishment of two invasive crustaceans (Copepoda: Harpacticoida) in the nearshore sands of Lake Michigan. Can. J. Fisheries Aquacult. Sci., 58, 1261–1264.CrossRefGoogle Scholar
Horwitz, T., 2000. Into the Blue: Boldly Going Where Captain Cook has Gone Before, Allen and Unwin, Crows Nest, 480 p.Google Scholar
Johnson, C.R., 2007. Seaweed invasions: conclusions and future directions. Bot. Mar., 50, 451–457.CrossRefGoogle Scholar
Karanovic, T., 2004. Subterranean copepoda from Arid Western Australia, Crustaceana Monographs 3, Brill, Leiden, 366 p.Google Scholar
Karanovic, T., 2005. Two new genera and three new species of subterranean cyclopoids (Crustacea, Copepoda) from New Zealand, with redescription of Goniocyclops silvestris Harding, 1958. Contr. Zool., 74, 223–254.Google Scholar
Karanovic, T., 2006. Subterranean copepods (Crustacea, Copepoda) from the Pilbara region in Western Australia, Issue 70 of Records of the Western Australian Museum, Western Australian Museum, Perth, 239 p.Google Scholar
Karanovic, T., 2008. Marine interstitial poecilostomatoida and cyclopoida (Copepoda) of Australia, Crustaceana Monographs 9, Brill, Leiden, 331 p.CrossRefGoogle Scholar
Karanovic, T. and Cooper, S.J.B, 2011. Third genus of parastenocarid copepods from Australia supported by molecular evidence (Harpacticoida: Parastenocarididae). Crustaceana Monographs 16, Brill, Leiden, 293–337.
Lee, C.E., 1999. Rapid and repeated invasions of fresh water by the copepod Eurytemora affinis. Evolution, 53, 1423–1434.CrossRefGoogle ScholarPubMed
Lee, C.E., Remfert, J.L. and Chang, Y.-M., 2007. Response to selection and evolvability of invasive populations. Genetica, 129, 179–192.CrossRefGoogle ScholarPubMed
Lee, C.E., Remfert, J.L. and Gelembiuk, G.W., 2003. Evolution of physiological tolerance and performance during freshwater invasions. Integr. Comp. Biol., 43, 439–449.CrossRefGoogle ScholarPubMed
Lefébure, T., Douady, C.J., Gouy, M. and Gibert, J., 2006. Relationship between morphological taxonomy and molecular divergence within Crustacea: Proposal of a molecular threshold to help species delimination. Mol. Phyl. Evol., 40, 435–447.CrossRefGoogle Scholar
Levin, D.A., 2003. The ecological transition in speciation. New Phytol., 161, 91–96.CrossRefGoogle Scholar
Machida, R.J., Miya, M.U., Nishida, M. and Nishida, S., 2004. Large-scale gene rearrangements in the mitochondrial genomes of two calanoid copepods Eucalanus bungii and Neocalanus cristatus (Crustacea), with notes on new versatile primers for the srRNA and COI genes. Gene, 332, 71–78.CrossRefGoogle Scholar
Matsuzaki, S.S., Usio, N., Takamura, N. and Washitani, I., 2009. Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia, 158, 673–686.CrossRefGoogle ScholarPubMed
May, G.E., Gelembiuk, G.W., Panov, V.E., Orlova, M.I. and Lee, C.E., 2006. Molecular ecology of zebra mussel invasions. Mol. Ecol., 15, 1021–1031.CrossRefGoogle ScholarPubMed
Merrit, T.J.S., Shi, L., Chase, M.C., Rex, M.A., Etter, R.J. and Quattro, J.M., 1998. Universal cytochrome b primers facilitate intraspecific studies in molluscan taxa. Mol. Mar. Biol. Biotechnol., 7, 7–11.Google Scholar
Ohtsuka, S., Itoh, H. and Mizushima, T., 2005. A new species of the calanoid copepod genus Centropages (Crustacea) collected from Shimizu Port, Middle Japan: Introduced or not? Plankt. Biol. Ecol., 52, 92–99.Google Scholar
Orsi, J.J. and Ohtsuka, S., 1999. Introduction of the Asian copepods Acartiella sinensis, Tortanus dextrilobatus (Copepoda: Calanoida), and Limnoithona tetraspina (Copepoda: Cyclopoida) to the San Francisco Estuary, California, USA. Plankt. Biol. Ecol., 46, 128–131.Google Scholar
Palumbi, S.R., Martin, A.P., Romano, S., McMillan, W.O., Stice, L. and Grabowski, G., 1991. The Simple Fool's Guide to PCR, Special Publication of the Department of Zoology, University of Hawaii, Honolulu, 47 p.Google Scholar
Pesole, G., Gissi, C., De Chirico, A. and Saccone, C., 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol., 48, 427–434.CrossRefGoogle ScholarPubMed
Pimentel, D., Lach, L., Zuniga, R. and Morrison, D., 2000. Environmental and economic costs of nonindigenous species in the United States. BioScience, 50, 53–65.CrossRefGoogle Scholar
Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol., 25, 1253–1256.CrossRefGoogle ScholarPubMed
Preston, C.D., Pearman, D.A. and Dines, T.D., 2002. New Atlas of the British Flora, Oxford University Press, Oxford, 910 p.Google Scholar
Rahel, F.J., 2007. Biogeographic barriers, connectivity and homogenization of freshwater faunas: it's a small world after all. Freshw. Biol., 52, 696–710.CrossRefGoogle Scholar
Reid, J.W. and Pinto-Coelho, R.M., 1994. An Afro-Asian continental copepod, Mesocyclops ogunnus, found in Brazil; with a new key to the species of Mesocyclops in South America and a review of intercontinental introduction of copepods. Limnologica, 24, 359–368.Google Scholar
Ross, D.J., Johnson, C.R. and Hewitt, C.L., 2006. Abundance of the introduced seastar, Asterias amurensis, and spatial variability in soft sediment assemblages in SE Tasmania: Clear correlation but complex interpretation. Estuar. Coast. Shelf Sci., 67, 695–707.CrossRefGoogle Scholar
Sakaguchi, S.O. and Ueda, H., 2010. A new species of Pseudodiaptomus (Copepoda: Calanoida) from Japan, with notes on the closely related P. inopinus Burckhardt, 1913 from Kyushu Island. Zootaxa, 2612, 52–68.Google Scholar
Schram, F.R., 2008. Does biogeography have a future in a globalized world with globalized faunas? Contr. Zool., 77, 127–133.Google Scholar
Schwenk, K., Sand, A., Boersma, M., Brehm, M., Mader, E., Offerhaus, D. and Spaak, P., 1998. Genetic markers, genealogies and biogeographic patterns in the Cladocera. Aquat. Ecol., 32, 37–51.CrossRefGoogle Scholar
Seddon, J.M., Baverstock, P.R. and Georges, A., 1998. The rate of mitochondrial 12S rRNA gene evolution is similar in freshwater turtles and marsupials. J. Mol. Evol., 46, 460–464.CrossRefGoogle ScholarPubMed
Spears, T., Abele, L.G. and Kim, W., 1992. The monophyly of brachyuran crabs: a phylogenetic study based on 18S rRNA. Syst. Biol., 41, 446–461.CrossRefGoogle Scholar
Stigall, A.L., 2007. Do invasive species cause extinction?: comparing invasion events during intervals of late Ordovician and late Devonian biotic turnover. In: GSA Denver Annual Meeting (28 September–1 October 2007), Paper No. 136-15.
Stock, J.K. and von Vaupel Klein, J.C., 1996. Mounting media revisited: the suitability of Reyne's fluid for small crustaceans. Crustaceana, 69, 749–798.CrossRefGoogle Scholar
Strain, E.M.A. and Johnson, C.R., 2009. Competition between and invasive urchin and commercially fished abalone: effect on body condition, reproduction and survivorship. Mar. Ecol. Prog. Ser., 377, 169–182.CrossRefGoogle Scholar
Suarez-Morales, E., McLelland, J. and Reid, J., 1999. The planktonic copepods of coastal saline ponds of the Cayman Islands with special reference to the occurrence of Mesocyclops ogunnus Onabamiro, an apparently introduced Afro-Asian cyclopoid. Gulf Res. Rep., 11, 51–55.Google Scholar
Tamura, K. and Nei, M., 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol., 10, 512–526.Google ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28, 2731–2739.CrossRefGoogle ScholarPubMed
Tavaré, S., 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura, R.M. (ed.), Some Mathematical Questions in Biology – DNA Sequence Analysis, American Mathematical Society, Providence, RI, 57–86.Google Scholar
Thompson, J.D., Higgins, D.G. and Gibson, T.J., 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673–4680.CrossRefGoogle Scholar
Winkler, G., Dodson, J.J. and Lee, C.E., 2008. Heterogeneity within the native range: population genetic analyses of sympatric invasive and noninvasive clades of the freshwater invading copepod Eurytemora affinis. Mol. Ecol., 17, 415–430.CrossRefGoogle ScholarPubMed
Zvyaginstev, A.Y. and Selifonova, J.P., 2008. Study of the ballast waters of commercial ships in the sea ports of Russia. Ross. Zhur. Bilog. Invaz., 2, 20–28.Google Scholar