Abstract
The predatory “killer shrimp” Dikerogammarus villosus invaded Britain from mainland Europe in 2010. Originating in the Ponto-Caspian region, this invader has caused significant degradation of European freshwater ecosystems by predating and competitively excluding native invertebrate species. In contrast to continental Europe, in which invasions occurred through the migration of large numbers of individuals along rivers and canals, the invasion of Great Britain must have involved long distance dispersal across the sea. This makes the loss of genetic diversity and of debilitating parasites more likely. Analysis of nuclear microsatellite loci and mitochondrial DNA sequences of D. villosus samples from the four known populations in Britain reveal loss of rare alleles, in comparison to reference populations from the west coast of continental Europe. Screening of the British D. villosus populations by PCR detected no microsporidian parasites, in contrast with continental populations of D. villosus and native amphipod populations, most of which are infected with microsporidia. These findings suggest that the initial colonisation of Great Britain and subsequent long distance dispersal within Britain were associated with genetic founder effects and enemy release due to loss of parasites. Such effects are also likely to occur during future long-distance dispersal events of D. villosus to Ireland or North America.
Similar content being viewed by others
References
Bacela-Spychalska K, Wattier RA, Genton C, Rigaud T (2012) Microsporidian disease of the invasive amphipod Dikerogammarus villosus and the potential for its transfer to local invertebrate fauna. Biol Invasions 14(9):1831–1842. doi:10.1007/s10530-012-0193-1
Boets P, Lock K, Tempelman D, Van Haaren T, Platvoet D, Goethals PLM (2012) First occurrence of the Ponto-Caspian amphipod Echinogammarus trichiatus (Martynov, 1932) (Crustacea: Gammaridae) in Belgium. BioInvasions Rec 1(2):115–120
Bojko J, Stebbing PD, Bateman KS, Meatyard JE, Bacela-Spychalska K, Dunn AM, Stentiford GD (2013) Baseline histopathological survey of a recently invading island population of ‘killer shrimp’, Dikerogammarus villosus. Dis Aquat Organ 106(3):241–253. doi:10.3354/dao02658
Casellato S, Visentin A, La Piana G (2007) The Predatory impact of Dikerogammarus villosus on fish. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats, vol 2. invading nature—springer series in invasion ecology, vol 2. Springer: Dordrecht, pp 495–506
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631. doi:10.1093/molbev/msl191
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7(8):721–733. doi:10.1111/j.1461-0248.2004.00616.x
Cristescu MEA, Witt JDS, Grigorovich IA, Hebert PDN, MacIsaac HJ (2004) Dispersal of the Ponto-Caspian amphipod Echinogammarus ischnus: invasion waves from the Pleistocene to the present. Heredity 92(3):197–203. doi:10.1038/sj.hdy.6800395
DAISIE (2009) Handbook of Alien species in Europe. Springer, Dordrecht
de Bij Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59(7):1159–1174. doi:10.1139/f02-098
Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B Methodol 39(1):1–38
Dick J, Platvoet D (1996) Intraguild predation and species exclusions in amphipods: the interaction of behaviour, physiology and environment. Freshw Biol 36(2):375–383. doi:10.1046/j.1365-2427.1996.00106.x
Dick JTA, Platvoet D (2000) Invading predatory crustacean Dikerogammarus villosus eliminates bath native and exotic species. Proc R Soc Lond Ser B Biol Sci 267(1447):977–983
Dick JTA, Platvoet D, Kelly DW (2002) Predatory impact of the freshwater invader Dikerogammarus villosus (Crustacea : Amphipoda). Can J Fish Aquat Sci 59(6):1078–1084. doi:10.1139/f02-074
Dunn AM, Torchin ME, Hatcher MJ, Kotanen PM, Blumenthal DM, Byers JE, Coon CAC, Frankel VM, Holt RD, Hufbauer RA, Kanarek AR, Schierenbeck KA, Wolfe LM, Perkins SE (2012) Indirect effects of parasites in invasions. Funct Ecol 26(6):1262–1274. doi:10.1111/j.1365-2435.2012.02041.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 Biotechnol 3(5):294–299
Grabowski M, Bacela K, Konopacka A (2007) How to be an invasive gammarid (Amphipoda : Gammaroidea)-comparison of life history traits. Hydrobiologia 590:75–84. doi:10.1007/s10750-007-0759-6
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hanfling B, Edwards F, Gherardi F (2011) Invasive alien Crustacea: dispersal, establishment, impact and control. Biocontrol 56(4):573–595. doi:10.1007/s10526-011-9380-8
Hatcher MJ, Dick JTA, Dunn AM (2012) Disease emergence and invasions. Funct Ecol 26(6):1275–1287. doi:10.1111/j.1365-2435.2012.02031.x
Hatcher MJ, Dunn AM (2011) Parasites in Ecological communities: from interactions to ecosystems. Ecology, Biodiversity and Conservation. Cambridge University Press, Cambridge
Hogg JC, Ironside JE, Sharpe RG, Hatcher MJ, Smith JE, Dunn AM (2002) Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR-RFLP. Parasitology 125:59–63. doi:10.1017/s0031182002001774
Holdich DM, Reeve ID (1991) Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquat Conserv Mar Freshw Ecosyst 1(2):139–158. doi:10.1002/aqc.3270010204
Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manage Aquat Ecosyst (394–395). doi:10.1051/kmae/2009025
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755. doi:10.1093/bioinformatics/17.8.754
Ironside JE, Smith JE, Hatcher MJ, Sharpe RG, Rollinson D, Dunn AM (2003) Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni. J Evol Biol 16(3):467–473. doi:10.1046/j.1420-9101.2003.00539.x
Ironside JE, Wilkinson TJ, Rock J (2008) Distribution and host range of the microsporidian Pleistophora mulleri. J Eukaryot Microbiol 55(4):355–362. doi:10.1111/j.1550-7408.2008.00338.x
Karaman GS, Pinkster S (1977) Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea, Amphipoda). 1. Gammarus pulex group and related species. Bijdragen Tot De Dierkunde 47(1):1–97
Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invasions 11(9):2009–2019. doi:10.1007/s10530-009-9498-0
Kelly DW, Muirhead JR, Heath DD, Macisaac HJ (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol Ecol 15(12):3641–3653. doi:10.1111/j.1365-294X.2006.03012.x
Krebes L, Blank M, Frankowski J, Bastrop R (2010) Molecular characterisation of the Microsporidia of the amphipod Gammarus duebeni across its natural range revealed hidden diversity, wide-ranging prevalence and potential for co-evolution. Infect Genet Evol 10(7):1027–1038. doi:10.1016/j.meegid.2010.06.011
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17(8):386–391. doi:10.1016/s0169-5347(02)02554-5
Lincoln RJ (1979) British Marine Amphipoda: Gammaridea. British Museum (Natural History), London
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89(3):238–247. doi:10.1093/jhered/89.3.238
MacNeil C, Platvoet D, Dick JTA, Fielding N, Constable A, Hall N, Aldridge D, Renals T, Diamond M (2010) The Ponto-Caspian ‘killer shrimp’, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles. Aquat Invasions 5(4):441–445. doi:10.3391/ai.2010.5.4.15
Ovcharenko MO, Bacela K, Wilkinson T, Ironside JE, Rigaud T, Wattier RA (2010) Cucumispora dikerogammari n. gen. (Fungi: Microsporldia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers. Parasitology 137(2):191–204. doi:10.1017/s0031182009991119
Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection [Ph.D. Thesis]. University of Dublin
Peakall R, Smouse P (2012) GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. doi:10.1093/bioinformatics/bts460
Piscart C, Bergerot B, Laffaille P, Marmonier P (2010) Are amphipod invaders a threat to regional biodiversity? Biol Invasions 12(4):853–863. doi:10.1007/s10530-009-9506-4
Piscart C, Mermillod-Blondin F, Maazouzi C, Merigoux S, Marmonier P (2011) Potential impact of invasive amphipods on leaf litter recycling in aquatic ecosystems. Biol Invasions 13(12):2861–2868. doi:10.1007/s10530-011-9969-y
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation—potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330. doi:10.1146/annurev.es.20.110189.001501
Ricciardi A (2001) Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Can J Fish Aquat Sci 58(12):2513–2525. doi:10.1139/cjfas-58-12-2513
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287(5459):1770–1774. doi:10.1126/science.287.5459.1770
Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates Incorporated, Sunderland
Slothouber Galbreath JGM, Smith JE, Becnel JJ, Butlin RK, Dunn AM (2010) Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Biol Invasions 12(1):191–209. doi:10.1007/s10530-009-9442-3
Slothouber Galbreath JGM, Smith JE, Terry RS, Becnel JJ, Dunn AM (2004) Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. Int J Parasitol 34(2):235–244. doi:10.1016/j.ijpara.2003.10.009
Strauss A, White A, Boots M (2012) Invading with biological weapons: the importance of disease-mediated invasions. Funct Ecol 26(6):1249–1261. doi:10.1111/1365-2435.12011
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. doi:10.1093/molbev/mst197
Terry RS, Smith JE, Dunn AM (1998) Impact of a novel, feminising microsporidium on its crustacean host. J Eukaryot Microbiol 45(5):497–501. doi:10.1111/j.1550-7408.1998.tb05106.x
Terry RS, Smith JE, Sharpe RG, Rigaud T, Littlewood DTJ, Ironside JE, Rollinson D, Bouchon D, MacNeil C, Dick JTA, Dunn AM (2004) Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc R Soc B Biol Sci 271(1550):1783–1789. doi:10.1098/rspb.2004.2793
Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalities and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. doi:10.1093/nar/22.22.4673
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421(6923):628–630. doi:10.1038/nature01346
Vainola R, Witt JDS, Grabowski M, Bradbury JH, Jazdzewski K, Sket B (2008) Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595:241–255. doi:10.1007/s10750-007-9020-6
van Riel MC, van der Velde G, Rajagopal S, Marguillier S, Dehairs F, de Vaate AB (2006) Trophic relationships in the Rhine food web during invasion and after establishment of the Ponto-Caspian invader Dikerogammarus villosus. Hydrobiologia 565:39–58. doi:10.1007/s10750-005-1904-8
Wattier RA, Beguet J, Gaillard M, Muller JC, Bollache L, Perrot-Minnot MJ (2006) Molecular markers for systematic identification and population genetics of the invasive Ponto-Caspian freshwater gammarid Dikerogammarus villosus (Crustacea, Amphipoda). Mol Ecol Notes 6(2):487–489. doi:10.1111/j.1471-8286.2006.01283.x
Wattier RA, Haine ER, Beguet J, Martin G, Bollache L, Musko IB, Platvoet D, Rigaud T (2007) No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos 116(11):1941–1953. doi:10.1111/j.2007.0030-1299.15921.x
Wilkinson TJ, Rock J, Whiteley NM, Ovcharenko MO, Ironside JE (2011) Genetic diversity of the feminising microsporidian parasite Dictyocoela: new insights into host-specificity, sex and phylogeography. Int J Parasitol 41(9):959–966. doi:10.1016/j.ijpara.2011.04.002
Yang GD, Short S, Kille P, Ford AT (2011) Microsporidia infections in the amphipod, Echinogammarus marinus (Leach): suggestions of varying causal mechanisms to intersexuality. Mar Biol 158(2):461–470. doi:10.1007/s00227-010-1573-7
Acknowledgments
This research project was supported by a Small Ecological Project Grant from the British Ecological Society. The authors would like to thank the Environment Agency for providing samples of D. villosus for use in this project.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arundell, K., Dunn, A., Alexander, J. et al. Enemy release and genetic founder effects in invasive killer shrimp populations of Great Britain. Biol Invasions 17, 1439–1451 (2015). https://doi.org/10.1007/s10530-014-0806-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-014-0806-y