Invasive cyprinid fish in Europe originate from the single introduction of an admixed source population followed by a complex pattern of spread

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Simon, Andrea ^a   Britton, Robert ^b   Gozlan, Rodolphe ^b   van Oosterhout, Cock ^d   Volckaert, Filip A M ^c   Hänfling, Bernd ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

^b BOURNEMOUTH UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B;

ANIMAL TISSUE; ARTICLE; BASE PAIRING; CONTROLLED STUDY; CYPRINIFORMES; CYTOCHROME B GENE; EUROPE; GENETIC DRIFT; GENETIC VARIABILITY; HAPLOTYPE; INVASIVE SPECIES; NATIVE SPECIES; NONHUMAN; NUCLEOTIDE SEQUENCE; POPULATION GENETICS; PSEUDORASBORA PARVA; SPECIES INVASION; UNINDEXED SEQUENCE; ANIMAL; BAYES THEOREM; GENETICS; INTRODUCED SPECIES; MOLECULAR EVOLUTION; PHYLOGENY; PHYLOGEOGRAPHY;

CYPRINIDAE; GOBIO; PSEUDORASBORA PARVA;

ANIMALS; BAYES THEOREM; CYPRINIDAE; EUROPE; EVOLUTION, MOLECULAR; GENETIC VARIATION; HAPLOTYPES; INTRODUCED SPECIES; PHYLOGENY; PHYLOGEOGRAPHY;

EID: 79958067231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018560     Document Type: Article

References (71)

1. Geller JB, Darling JA, Carlton JT, (2010) Genetic Perspectives on Marine Biological Invasions. Annual Review of Marine Science 2: 367-393 (DOI:10.1146/annurev.marine.010908.163745).
2. Le Roux J, Wieczorek AM, (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Annals of Applied Biology 154: 1-17 (DOI: 10.1111/j.1744-7348.2008.00280.x).
3. Hänfling B, (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. Journal of Fish Biology 71: 115-135 (DOI: 10.1111/j.1095-8649.2007.01685.x).
4. Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A, (2010): Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104: 88-99 (DOI:10.1038/hdy.2009.92).
5. Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath D, et al. (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Molecular Ecology 17: 1020-1035 (DOI: 10.1111/j.1365-294X.2008.03669.x).
6. Lee CE, (2002) Evolutionary genetics of invasive species. Trends in Ecology & Evolution 17: 386-391 (DOI:10.1016/S0169-5348(02)02554-5).
7. Brown JE, Stepien CA, (2008) Ancient divisions, recent expansions: Phylogeography and population genetics of the round goby Apollonia melanostoma across Eurasia. Molecular Ecology 11: 2598-615 (DOI: 10.1111/j.1365-294X.2008.03777.x).
8. Nei M, Maruyama T, Chakraborty R, (1975): The bottleneck effect and genetic variability in populations. Evolution 29: 1-10.
9. Williamson M, Fitter A, (1996) The characteristics of successful invaders. Biological Conservation 78: 163-170 (DOI:10.1016/0006-3207(96)00025-0).
10. Frankham R, (2005) Genetics and extinction. Biological Conservation 126: 131-140 (DOI:10.1016/j.biocon.2005.05.002).
11. Poulin J, Weller SG, Sakai AK, (2005) Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii. Diversity and Distributions 11: 241-247 (DOI: 10.1111/j.1366-9516.2005.00136.x).
12. Ficetola GF, Bonin A, Miaud C, (2008) Population genetics reveals origin and number of founders in a biological invasion. Molecular Ecology 17: 773-782 (DOI: 10.1111/j.1365-294X.2007.03622.x).
13. Roman J, Darling JA, (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology & Evolution 22: 454-464 (DOI:10.1016/j.tree.2007.07.002).
14. Kelly DW, Muirhead JR, Heath DD, Macisaac HJ, (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish water. Molecular Ecology 15: 3641-3653 (DOI: 10.1111/j.1365-294X.2006.03012.x).
15. Haynes GD, Gilligan DM, Grewe P, Nicholas FW, (2009) Population genetics and management units of invasive common carp Cyprinus carpio in the Murray-Darling Basin, Australia. Journal of Fish Biology 75: 295-320 (DOI: 10.1111/j.1095-8649.2009.02276.x).
16. Zidana H, Turner GF, van Oosterhout C, Hänfling B, (2009) Elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization. Molecular Ecology 18: 4380-4389 (DOI: 10.1111/j.1365-294X.2009.04362.x).
17. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, et al. (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177-181 (DOI:10.1038/nature02807).
18. Rosenthal DM, Ramakrishnan AP, Cruzan MB, (2008) Evidence for multiple sources of invasion and intraspecific hybridization in Brachypodium sylvaticum (Hudson) Beauv. in North America. Molecular Ecology 17: 4657-4669 (DOI: 10.1111/j.1365-294X.2008.03844.x).
19. Gozlan RE, Pinder AC, Shelley J, (2002) Occurrence of the Asiatic cyprinid Pseudorasbora parva in England. Journal of Fish Biology 61: 298-300 (DOI: 10.1111/j.1095-8649.2002.tb01755.x).
20. Gozlan RE, Britton JR, Cowx I, Copp GH, (2010a) Current knowledge on non-native freshwater fish introductions. (Review) Journal of Fish Biology 76: 751-786 (DOI: 10.1111/j.1095-8649.2010.02566.x).
21. Rosecchi E, Thomas F, Crivelli AJ, (2001): Can life-history traits predict the fate of introduced species? A case study on two cyprinids in southern France. Freshwater Biology 46: 845-853 (DOI: 10.1046/j.1365-2427.2001.00715.x).
22. Gozlan RE, Andreou D, Asaeda T, Beyer K, Bouhadad R, et al. (2010b): Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish and Fisheries 11: 315-340 (DOI: 10.1111/j.1467-2979.2010.00361.x).
23. Britton JR, Davies GD, Harrod C, (2010): Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK. Biological Invasions 12: 1533-1542 (DOI 101007/s10530-009-9566-5).
24. Britton JR, Davies GD, Brazier M, Pinder AC, (2007): A case study on the population ecology of a topmouth gudgeon Pseudorasbora parva population in the UK and the implications for native fish communities. Aquatic Conservation: Marine & Freshwater Ecosystems 17: 749-759 (DOI: 101002/aqc809).
25. Benejam L, Carol J, Alcaraz C, Garcia-Berthou E, (2005) First record of the common bream (Abramis brama) introduced to the Iberian Peninsula. Limnetica 24: 273-274.
26. Vidal O, Garcia-Berthou E, Tedesco PA, Garcia-Marin J, (2010) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biological Invasions 12: 841-851 (DOI 101007/s10530-009-9505-5).
27. Cesco H, Lambert A, Crivelli AJ, (2001) Pseudorasbora parva (téléostéen Cyprinidae) espèce invasive nouvel agent du maintien et de la dissémination de l'anguillicolose en France? Parasite 8: 75-76.
28. Gozlan RE, St-Hilaire S, Feist SW, Martin P, Kent ML, (2005) Biodiversity - disease threat to European fish. Nature 435: 1046 (DOI101038/4351046a).
29. Gozlan RE, Whipps CM, Andreou D, Arkush KD, (2009) Identification of a rosette-like agent as Sphaerothecum destruens a multi-host fish pathogen. International Journal for Parasitology 39: 1055-1058 (DOI101016/jijpara200904012).
30. Berg LS, (1949) Ryby presnych vod SSSR i sopredelnych stran 2 ss 477-925 Izd AN SSSR Moskva-Leningrad.
31. Bǎnǎrescu P, (1999) Pseudorasbora parva (Temmnick et Schlegel 1846) In: Bǎnǎrescu P, editors. The freshwater fishes of Europe 5I Cyprinidae 2/I Aula Verl Wiesbaden.
32. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, et al. (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (hotshot). Biotechniques 29: 52-54.
33. Briolay J, Galtier N, Brito RM, Bouvet Y, (1998) Molecular Phylogeny of Cyprinidae Inferred from cytochrome b DNA Sequences. Molecular Phylogenetics and Evolution 9: 100-108 (DOI101006/mpev19970441).
34. Ewing B, Hillier L, Wendl MC, Green P, (1998) 'Base calling of automated sequencer traces using PHRED I Accuracy assessment'. Genome Research 8 (DOI101101/gr83175): 175-185.
35. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4 Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599 (DOI101093/molbev/msm092).
36. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882 (DOI 101093/nar/25244876).
37. Tamura K, Nei M, Kumar S, (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences U S A 101: 11030-11035 (DOI101073/pnas0404206101).
38. Stamatakis A, Hoover P, Rougemont J, (2008) A Fast Bootstrapping Algorithm for the RAxML Web-Servers. Systematic Biology 57: 758-771 (DOI 101080/10635150802429642).
39. Liu HZ, Yang JQ, Tang QY, (2010) Estimated evolutionary tempo of East Asian gobionid fishes (Teleostei Cyprinidae) from mitochondrial DNA sequence data. Chinese Science Bulletin 55: 1501-1510.
40. Tang KL, Agnew MK, Hirt MV, et al. (2010) Systematics of the subfamily Danioninae (Teleostei Cypriniformes Cyprinidae) Molecular Phylogenetics and Evolution 57: 189-214 (DOI101016/jympev201005021).
41. Bandelt HJ, Forster P, Röhl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48.
42. Broughton RE, Stanley SE, Durrett RT, (2000) Quantification of homoplasy for nucleotide transitions and transversions and a re-examination of assumptions in weighted phylogenetic analysis. Systematic Biology 49: 617-627 (DOI 101080/106351500750049734).
43. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic Local Alignment Search Tool. Journal of Molecular Biology 215: 403-410 (DOI101006/jmbi199 09999).
44. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R, (2003) DnaSP DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497 (DOI 101093/bioinformatics/btg359).
45. Nei M, Jin L, (1989) Variances of the average numbers of nucleotide substitutions within and between populations. Molecular Biology and Evolution 6: 290-300.
46. Lynch M, Crease TM, (1990) The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution 7: 377-394.
47. Hudson RR, (1990) Gene genealogies and the coalescent process. In: Futuyama D, Antonovics J, editors. Oxford Surveyin Evolutionary Biology Vol 7 Oxford University Press Oxford pp. 1-42.
48. Beerli P, (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22: 341-345 (DOI101093/bioinformatics/bti803).
49. Kimura M, (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
50. Ramachandran S, Deshpande O, Roseman CC, Rosenberg NA, Feldman MW, et al. (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Nat Acad Sci U S A 102: 15942-15947 (DOI 101073/pnas0507611102).
51. Herborg LM, Weetman D, van Oosterhout C, Hänfling B, (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader the Chinese mitten crab Eriocheir sinensis. Molecular Ecology 16: 231-242 (DOI 101111/j1365-294X200603133x).
52. Wright S, (1943) Isolation by distance. Genetics 28: 114-138.
53. Jensen JL, Bohonak AJ, Kelley ST, (2005) Isolation by distance web service. BMC Genetics 6: 13 v316 http://ibdws.sdsu.edu/.
54. Bǎnǎrescu P, Nalbant T, (1965) Studies on the systematics of Gobioninae (Pisces Cyprinidae). Rev Roum de Biol Ser de Zoologie 10: 219-229.
55. Cornuet J, Santos F, Beaumont MA, Robert CP, Marin J, et al. (2008) Inferring population history with DIY ABC a user-friendly approach to approximate Bayesian computation. Bioinformatics 24: 2713-2719 (DOI101093/bioinformatics/btn514).
56. Durand JD, Tsigenopoulos CS, Unlu E, Berrebi P, (2002) Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from cytochrome b DNA- Evolutionary significance of this region. Molecular Phylogenetics and Evolution 25: 218-218 (DOI101006/mpev20011040).
57. Watanabe K, Iguchi K, Hosoya K, Nishida M, (2000) Phylogenetic relationships of the Japanese minnows Pseudorasbora (Cyprinidae) as inferred from mitochondrial 16S rRNA gene sequences. Ichthyological research 47: 43-50 (DOI 10.1007/BF02674312).
58. Hänfling B, Brandl R, (1998) Genetic differentiation of the bullhead Cottus gobio L across watersheds in central Europe evidence for two taxa. Heredity 80: 110-117 (DOI101046/j1365-2540199800279x).
59. Hänfling B, Kollmann J, (2002) An evolutionary perspective of biological invasions. Trends in Ecology & Evolution 17: 545-546 (DOI101016/S0169-5347(02)02644-7).
60. Barson NJ, Cable J, van Oosterhout C, (2009) Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago evidence for a dynamic source-sink metapopulation structure founder events and population bottlenecks. Journal of Evolutionary Biology 22: 485-497 (DOI101111/j1420-9101200801675x).
61. Willing EM, Bentzen P, van Oosterhout C, Hoffmann M, Cable J, et al. (2010) Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Molecular Ecology 19: 968-984 (DOI 101111/j1365-294X201004528x).
62. Saillant E, Patton JC, Gold JR, (2005) Genetic Variation Kinship and Effective Population Size in a Captive Population of the Endangered Cape Fear Shiner Notropis mekistocholas. Copeia 1: 20-28 (DOI 101643/CG-04-200R1).
63. Hänfling B, Weetman D, (2006) Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the River Sculpin Cottus gobio. Genetics 173: 1487-1501 (DOI101534/genetics105054296).
64. Yang L, He S, (2008) Phylogeography of the freshwater catfish Hemibagrus guttatus (Siluriformes Bagridae) Implications for South China biogeography and influence of sea-level changes. Molecular Phylogenetics and Evolution 49: 393-398 (DOI101016/jympev200805032).
65. Lin C, Lin H, Wang J, Chao S, Chiang T, (2010) Phylogeography of Hemibarbus labeo (Cyprinidae) secondary contact of ancient lineages of mtDNA. Zoologica Scripta 39: 23-35 (DOI 101111/j1463-6409200900407x).
66. Hua X, Wang W, Yin W, He Q, Jin B, et al. (2009) Phylogeographical analysis of an estuarine fish Salanx ariakensis (Osmeridae Salanginae) in the north-western Pacific. Journal of Fish Biology 75: 354-367 (DOI 101111/j1095-8649200902323x).
67. Jamandre BW, Durand JD, Tzeng WN, (2009) Phylogeography of the flathead mullet Mugil cephalus in the north-west Pacific as inferred from the mtDNA control region. Journal of Fish Biology 75: 393-407 (DOI 101111/j1095-8649200902332x).
68. Liu J, Brown CL, Yang T, (2009) Population genetic structure and historical demography of grey mullet Mugil cephalus along the coast of China inferred by analysis of the mitochondrial control region. Biochemical Systematics and Ecology 37: 556-566 (DOI101016jbse200909002).
69. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, et al. (2000) Effect of aquaculture on world fish supplies. Nature 405: 1017-1024 (DOI101038/35016500).
70. Gozlan RE, Beyer K, (2006) Hybridisation between Pseudorasbora parva and Leucaspius delineatus. Folia Zoologica 55: 53-60.
71. Roman J, (2006) Diluting the founder effect cryptic invasions expand a marine invader's range. Proceedings of the Royal Society B 273: 2453-2459 (DOI101098/rspb20063597).