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Pathways of cryptic invasion in a fish parasite traced using coalescent analysis and epidemiological survey

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Abstract

Introduced species have the potential to outperform natives via the introduction of new parasites to which the native ecosystem is vulnerable. Cryptic diversity within an invasive species can obscure invasion patterns and confound proper management measures. The aim of this study is to use coalescent theory based methodology to trace recent routes of invasion in populations of Ligula intestinalis, a globally distributed fish parasite possessing both native and recently introduced populations in North Africa. Molecular analyses of mitochondrial DNA discerned a pronounced genetic divergence between introduced and native populations. Distribution of mitochondrial haplotypes demonstrated common origin of European populations with North African parasites sampled from introduced fish species in Tunisia. To test the suggested pathway of introduction, microsatellite data were examined in a model-based coalescent analysis using the software MIGRATE, where Europe to Tunisia direction of migration was favoured over alternative hypotheses of gene flow. Specificity of Tunisian populations to different host species was assessed in an epidemiologic survey confirming prevailing host-based division between introduced and native parasites in North Africa. This approach combining advanced analysis of molecular markers with host-specificity data allows revealing the evolution of host-parasite interactions following biological invasion and provides basis for devising future management measurements.

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References

  • Arme C (1997) Ligulosis in two cyprinid hosts: Rutilus rutilus and Gobio gobio. Helmithologia 34:191–196

    Google Scholar 

  • Ascunce MS, Yang C–C, Oakey J, Calcaterra L, Wu W-J, Shih C-J, Goudet J, Ross KG, Shoemaker DW (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068

    Article  CAS  PubMed  Google Scholar 

  • Bahri-Sfar L, Haddaoui N, Bouzid W, Essetti I, Qninba A, Ben Hassine OK (2010) Compared parasitic infection of Ligula intestinalis (Cestoda: Diphyllobothridae) in Cyprinidae species: Rutilus rubilio and Scardinius erythrophthalmus in two dam reserves in Tunisia. Parasite 17:241–250

    Article  CAS  PubMed  Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345. doi:10.1093/bioinformatics/bti803

    Article  CAS  PubMed  Google Scholar 

  • Beerli P (2009) How to use migrate or why are markov chain monte carlo programs difficult to use? In: Bertorelle G, Bruford MW, Hauffe HC et al (eds) Population genetics for animal conservation. Cambridge University Press, Cambridge, pp 42–79

    Google Scholar 

  • Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326. doi:10.1534/genetics.109.112532

    Article  PubMed  Google Scholar 

  • Blum MGB, Damerval C, Manel S, Francois O (2004) Brownian models and coalescent structures. Theor Popul Biol 65:249–261

    Article  PubMed  Google Scholar 

  • Bouzid W, Lek S, Mace M, Ben Hassine OK, Etienne R, Legal L, Loot G (2008a) Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. J Zool Syst Evol Res 46:289–296

    Article  Google Scholar 

  • Bouzid W, Štefka J, Hypša V, Lek S, Scholz T, Legal L, Ben Hassine OK, Loot G (2008b) Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int J Parasitol 38:1465–1479

    Article  CAS  PubMed  Google Scholar 

  • Brown JE, Stepien CA (2010) Population genetic history of the dreissenid mussel invasions: expansion patterns across North America. Biol Invasions 12:3687–3710

    Article  Google Scholar 

  • Brown SP, Loot G, Grenfell BT, Guégan JF (2001) Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123:519–529

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Carter V, Pierce R, Dufour S, Arme C, Hoole D (2005) The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 130:939–945

    Article  CAS  PubMed  Google Scholar 

  • Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. doi:10.1016/j.tree.2005.01.003

    Article  PubMed  Google Scholar 

  • Clayton DH, Al-Tamimi S, Johnson KP (2003) The ecological basis of coevolutionary history In: Page RDM (ed) Tangled trees: phylogeny, cospeciation and coevolution. University of Chicago Press, Chicago, pp 310–341

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Dejen E, Vijverberg J, Sibbing FA (2006) Spatial and temporal variation of cestode infection and its effects on two small barbs (Barbus humilis and B. tanapelagius) in Lake Tana, Ethiopia. Hydrobiologia 556:109–117

    Article  Google Scholar 

  • Djemali I (2005) Évaluation de la biomasse piscicole dans les plans d’eau douce tunisiens: approches analytique et acoustique. Institut National Agronomique de Tunisie

  • Djemali I, Kraïem MM, Cadic N, Proteau JP, El Abed A, Jarboui O (2003) Evaluation de la biomasse piscicole en eau douce par écho prospection: application à la retenue de Sidi Salem. Bull Inst Natl Sci Technol Mer 30:23–32

    Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x

    Article  CAS  PubMed  Google Scholar 

  • Dubinina MN (1980) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. Amerind Publishing Co, New Delhi

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) 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. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  CAS  PubMed  Google Scholar 

  • Fujisaki I, Pearlstine EV, Mazzotti FJ (2010) The rapid spread of invasive Eurasian collared doves Streptopelia decaocto in the continental USA follows human-altered habitats. Ibis 152:622–632

    Article  Google Scholar 

  • Goka K, Yokoyama J, Une Y, Kuroki T, Suzuki K, Nakahara M, Kobayashi A, Mizutani T, Inaba S, Hyatt AD (2009) Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Mol Ecol 18:4757–4774

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Hoole D, Carter V, Dufour S (2010) Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model? Parasitology 137:425–438

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jeffreys H (1961) The theory of probability. Oxford University Press, New York. (3rd edition 1998)

  • Kass RE, Raftery AE (1995) Bayes Factors. J Am Stat Assoc 90:773–779

    Article  Google Scholar 

  • Kennedy CR, Shears PC, Shears JA (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123:257–269

    Article  CAS  PubMed  Google Scholar 

  • Khalil L, Polling L (1971) Checklist of the helminth parasites of african freshwater fishes. In: Farnham R (ed). Commonwealth Agricultural Bureaux publishing, Slough, pp 80

  • Khamis FM, Karam N, Ekesi S, De Meyer M, Bonomi A, Gomulski LM, Scolari F, Gabrieli P, Siciliano P, Masiga D, Kenya EU, Gasperi G, Malacrida AR, Guglielmino CR (2009) Uncovering the tracks of a recent and rapid invasion: the case of the fruit fly pest Bactrocera invadens (Diptera: Tephritidae) in Africa. Mol Ecol 18:4798–4810

    Article  CAS  PubMed  Google Scholar 

  • Kraïem M (1983) Les poissons d’eau douce de Tunisie: inventaire commenté et répartition géographique. Bull Inst Natl Sci Tech Océanogr Pêche Salammbô 10:107–124

    Google Scholar 

  • Kraïem M (1991) Étude Eco-biologique de principales espèces de poissons des retenues des barrages de Sidi Salem, Bir M’Cherga, Mellègue, Bouhertma, Nebhana et Sidi Saad. Rapports Techniques Projet Tuniso-Allemend de pêche continentale 11: 48

  • Králová-Hromadová I, Bazsalovicsová E, Štefka J, Špakulová M, Vávrová S, Szemes T, Tkach V, Trudgett A, Pybus M (2011) Multiple origins of European populations of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae), a liver parasite of ruminants. Int J Parasitol 41:373–383

    Article  PubMed  Google Scholar 

  • Li J, Liao X (2003) The taxonomic status of Digramma (Pseudophyllidae: Ligulidae) inferred from DNA sequences. J Parasitol 89:792–799

    Article  CAS  PubMed  Google Scholar 

  • Li J, Liao X, Yang H (2000) Molecular characterization of a parasitic tapeworm (Ligula) based on DNA sequences from formalin-fixed specimens. Biochem Genet 38:309–322

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Google Scholar 

  • Light JE, Hafner MS (2008) Codivergence in heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Syst Biol 57:449–465

    Article  PubMed  Google Scholar 

  • Loot G, Lek S, Brown SP, Guégan J-F (2001a) Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea). J Parasitol 87:1002–1010

    CAS  PubMed  Google Scholar 

  • Loot G, Lek S, Dejean D, Guégan J-F (2001b) Parasite-induced mortality in three host populations of the roach Rutilus rutilus (L.) by the tapeworm Ligula intestinalis (L.). Ann Limnol Int J Limnol 37:151–159

    Article  Google Scholar 

  • Loot G, Aulagnier S, Lek S, Thomas F, Guégan J-F (2002) Experimental demonstration of a behavioural modification in a cyprinid fish, Rutilus rutilus (L.), induced by a parasite, Ligula intestinalis (L.). Can J Zool 80:738–743

    Article  Google Scholar 

  • Loot G, Park Y-S, Lek S, Brosse S (2006) Encounter rate between local populations shapes host selection in complex parasite life cycle. Biol J Lin Soc 89:99–106

    Article  Google Scholar 

  • Losse G, Nau W, Winter M (1991) Le développement de la pêche en eau douce dans le nord de la Tunisie: Projet de la coopération technique Tuniso-Allemande. Utilisation des barrages pour la pisciculture, GTZ Gmbh

    Google Scholar 

  • Manilla G, Albertini D, Falasca MP (1984) Ligula intestinalis (L., 1758) Gmelin, 1790 (Cestoda: Ligulidae) in Rutilus rubilio (Pisces: Cyprinidae) of Campotosto Lake. Riv Parasitol 45:263–279

    Google Scholar 

  • Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J Parasitol 68:131–133

    Google Scholar 

  • Meddour A (1988) Parasites of freshwater fishes from Lake Oubeira. Dissertation, Department of Zoology, The University of Liverpool, UK, Algeria

    Google Scholar 

  • Meddour A, Rouabhi A, Meddour-Bouderda K, Loucif N, Remili A, Khataly Y (2005) Expérimentations sur la reproduction artificielle de Sander lucioperca, Hypophthalmichthys molitrix et Aristichthys nobilis en Algérie. Sci Technol 23:63–71

    Google Scholar 

  • Mergeay J, Verschuren D, De Meester L (2006) Invasion of an asexual American water flea clone throughout Africa and rapid displacement of a native sibling species. Proc R Soc Lond Biol 273:2839–2844

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nuismer SL, Thompson JN (2006) Coevolutionary alternation in antagonistic interactions. Evolution 60:2207–2217

    PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Center Uppsala University

  • Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

    Article  CAS  PubMed  Google Scholar 

  • Olson PD, Littlewood DTJ, Griffiths D, Kennedy CR, Arme C (2002) Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J Helminthol 76:171–174

    Article  CAS  PubMed  Google Scholar 

  • Perea S, Böhme M, Zupancic P, Freyhof J, Sanda R, Özulug M, Abdoli A, Doadrio I (2010) Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evol Biol 10:265

    Article  PubMed  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Posada D (2004) Collapse (Version 1.2). A tool for collapsing sequences to haplotypes. http://darwin.uvigo.es/

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton

  • Prenter J, Macneil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond A (2005) Tracer. Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed.ac.uk/software/tracer/

  • Rushton SP, Lurz PWW, Gurnell J, Nettleton P, Bruemmer C, Shirley MDF, Sainsbury AW (2006) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidemiol Infect 134:521–533

    Article  CAS  PubMed  Google Scholar 

  • Sasal P, Taraschewski H, Grondin H, Valade P, Wielgoss S, Moravec F (2008) Parasite communities in eels of the Island of Reunion (Indian Ocean): a lesson in parasite introduction. Parasitol Res 102:1343–1350

    Article  PubMed  Google Scholar 

  • Štefka J, Gilleard JS, Grillo V, Hypša V (2007) Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea). Mol Ecol Notes 7:794–796

    Article  Google Scholar 

  • Štefka J, Hypša V, Scholz T (2009) Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Mol Ecol 18:1187–1206

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Patrick A, Brennan EB, Burckhardt DH, Baumann P (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66:2898–2905

    Article  CAS  PubMed  Google Scholar 

  • Therriault TW, Orlova MI, Docker MF, Macisaac HJ, Heath DD (2005) Invasion genetics of a freshwater mussel (Dreissena rostriformis bugensis) in eastern Europe: high gene flow and multiple introductions. Heredity 95:16–23

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

  • Van Riper C III, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344

    Article  Google Scholar 

  • Wattier RA, Haine ER, Beguet J, Martin G, Bollache L, Muskó IB, Platvoet D, Rigaud T (2007) No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos 116:1941–1953

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wielgoss S, Taraschewski H, Meyer A, Wirth T (2008) Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Mol Ecol 17:3478–3495

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Abdessalem Arab, Sonia Thabet, Abdelkader Lounaci and Mejdeddine Kraïem for providing part of the Ligula samples. The study was supported by the Embassy of France in Tunisia and by the Czech Science Foundation (projects No. 206/08/1019, 506/12/1632). Research stay of JŠ in the Natural History Museum was funded by Marie Curie Fellowship (project no. 235123, FP7-PEOPLE-IEF-2008). PB was partly supported by American National Science Foundation grants DEB 0822626 and DEB 1145999. Part of the computations were performed using the computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum (provided under the programme Projects of Large Infrastructure for Research, Development, and Innovations, LM2010005) and using the Florida State University High Performance Computing facility.

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Bouzid, W., Štefka, J., Bahri-Sfar, L. et al. Pathways of cryptic invasion in a fish parasite traced using coalescent analysis and epidemiological survey. Biol Invasions 15, 1907–1923 (2013). https://doi.org/10.1007/s10530-013-0418-y

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