Skip to main content

Advertisement

SpringerLink
Log in

Population genetics of pike, genus Esox (Actinopterygii, Esocidae), in Northern Italy: evidence for mosaic distribution of native, exotic and introgressed populations

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

An Erratum to this article was published on 14 June 2017

Abstract

Esox flaviae represents the native esocid species of the Italian peninsula at present potentially highly threatened by the diffusion of exotic E. lucius. Here, we present a novel mtDNA (N = 272) and microsatellite (N = 275) dataset including 13 test and 3 reference samples, aimed to delineate the distribution of the native as well as the exotic species and to unravel potential introgressive hybridisation between the two species in Northern Italy. We highlight a complex mosaic distribution of both species, with contrasting occurrence even between neighbouring sites. Significant genetic substructure is still observed within E. flaviae, while the dispersal of the invader seems to be promoted by restocking actions. In addition, we prove the existence of introgressive hybridisation between native and exotic pikes. Here, gender-biased hybridisation is suggested, with native E. flaviae constituting the predominant ‘mother species’ in the hybridisation process. Finally, we underline the need for a revision of fisheries management regulations, for which a nation-wide and exhaustive genetic screening in the near future should build the scientific basis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aguilar, A., J. D. Banks, K. F. Levine & R. K. Wayne, 2005. Population genetics of northern pike (Esox lucius) introduced into Lake Davis, California. Canadian Journal of Fisheries and Aquatic Sciences 62: 1589–1599.

    Article  CAS  Google Scholar 

  • Akaike, H., 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.

    Article  Google Scholar 

  • Allendorf, F. W. & G. Luikart, 2007. Conservation and the Genetics of Populations. Blackwell Publishing, Oxford.

    Google Scholar 

  • Anderson, E. C. & E. A. Thompson, 2002. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160: 1217–1229.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baars, M., E. Mathes, H. Stein, & U. Steinhörster, 2001. Die Äsche. Die Neue Brehm-Bücherei, Westarp Wissenschaften, Hohenwarsleben

  • Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Bekkevold, D., L. Jacobsen, J. Hemmer-Hansen, S. Berg & C. Skov, 2015. From regionally predictable to locally complex population structure in a freshwater top predator: river systems are not always the unit of connectivity in Northern Pike Esox Lucius. Ecology of Freshwater Fish 24: 305–316.

    Article  Google Scholar 

  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996–2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France.

  • Bianco, P. G., 2014. An update on the status of native and exotic freshwater fishes of Italy. Journal of Applied Ichthyology 30: 62–77.

    Article  Google Scholar 

  • Bianco, P. G. & G. B. Delmastro, 2011. Recenti novità tassonomiche riguardanti i pesci d’acqua dolce autoctoni in Italia e descrizione di una nuova specie di luccio. Researches on Wildlife Conservation, vol 2 (suppl.), IGF Publishing, USA, pp. 14.

  • Crossman, E. J. & K. Buss, 1965. Hybridization in the family Esocidae. Journal of the Fisheries Research Board of Canada 22: 1261–1292.

    Article  Google Scholar 

  • Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delmastro, G. B., G. Boano, P. Lo Conte & S. Fenoglio, 2015. Great cormorant predation on Cisalpine pike: a conservation conflict. European Journal of Wildlife Research 61: 743–748.

    Article  Google Scholar 

  • Denys, G. P. J., A. Dettai, H. Persat, M. Hautecoeur & P. Keith, 2014. Morphological and molecular evidence of three species of pikes Esox spp. (Actinopterygii, Esocidae) in France, including the description of a new species. Comptes Rendus Biologies 337: 521–534.

    Article  PubMed  Google Scholar 

  • Earl, D. A. & B. M. vonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.

    Article  Google Scholar 

  • Epifanio, J. & D. Philipp, 2001. Simulating the extinction of parental lineages from introgressive hybridization: the effects of fitness, initial proportions of parental taxa, and mate choice. Reviews in Fish Biology and Fisheries 10: 339–354.

    Article  Google Scholar 

  • Eschbach, E. & S. Schoning, 2013. Identification of high-resolution microsatellites without a priori knowledge of genotypes using a simple scoring approach. Methods in Ecology and Evolution 4: 1076–1082.

    Article  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L. & M. Slatkin, 1998. Incorporating genotypes of relatives into a test of linkage disequilibrium. The American Journal of Human Genetics 62: 171–180.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Article  PubMed  Google Scholar 

  • Gandolfi, A., D. Fontaneto, M. Natali & L. Lucentini, 2016. Mitochondrial genome of Esox flaviae (Southern pike): announcement and comparison with other Esocidae. Mitochondrial DNA Part A 27: 3037–3038.

    CAS  Google Scholar 

  • Genovesi, P., P. Angelini, E. Bianchi, E. Dupré, S. Ercole, V. Giacanelli, F. Ronchi & F. Stoch, 2014. Specie e habitat di interesse comunitario in Italia: distribuzione, stato di conservazione e trend. ISPRA, Serie Rapporti, 194/2014.

  • Goudet, J., 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86: 485–486.

    Article  Google Scholar 

  • Gozlan, R. E., D. Andreou, T. Asaeda, K. Beyer, R. Bouhadad, D. Burnard, N. Caiola, P. Cakic, V. Djikanovic, H. R. Esmaeili, I. Falka, D. Golicher, A. Harka, G. Jeney, V. Kováč, J. Musil, A. Nocita, M. Povz, N. Poulet, T. Virbickas, C. Wolter, A. S. Tarkan, E. Tricarico, T. Trichkova, H. Verreycken, A. Witkowski, C. G. Zhang, I. Zweimueller & J. R. Britton, 2010. Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish & Fisheries 11: 315–340.

    Article  Google Scholar 

  • Gratton, P., G. Allegrucci, A. Gandolfi & V. Sbordoni, 2013. Genetic differentiation and hybridization in two naturally occurring sympatric trout Salmo spp. forms from a small karstic lake. Journal of Fish Biology 82: 637–657.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guo, S. W. & E. A. Thompson, 1992. Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48: 361–372.

    Article  CAS  PubMed  Google Scholar 

  • Hansen, M. M., J. B. Taggart & D. Meldrup, 1999. Development of new VNTR markers for pike and assessment of variability at di- and tetranucleotide repeat microsatellite loci. Journal of Fish Biology 55: 183–188.

    Article  CAS  Google Scholar 

  • Hansen, M. M., D. E. Ruzzante, E. E. Nielsen & K.-L. D. Mensberg, 2001. Brown trout (Salmo trutta) stocking impact assessment using microsatellite DNA markers. Ecological Applications 11: 148–160.

    Article  Google Scholar 

  • Harvey, B., 2009. A biological synopsis of northern pike (Esox lucius). Manuscript Report of Fisheries and Aquatic Sciences, 2885.

  • Hermoso, V. & M. Clavero, 2011. Threatening processes and conservation management of endemic freshwater fish in the Mediterranean basin: a review. Marine and Freshwater Research 62: 244–254.

    Article  CAS  Google Scholar 

  • Holleley, C. E. & P. G. Geerts, 2009. Multiplex Manager 1.0: a crossplatform computer program that plans and optimizes multiplex PCR. BioTechniques 46: 511–517.

    Article  CAS  PubMed  Google Scholar 

  • Huhn, D., K. Lubke, C. Skov & R. Arlinghaus, 2014. Natural recruitment, density-dependent juvenile survival, and the potential for additive effects of stock enhancement: an experimental evaluation of stocking northern pike (Esox lucius) fry. Canadian Journal of Fisheries and Aquatic Sciences 71: 1508–1519.

    Article  Google Scholar 

  • Huson, D. H. & D. Bryant, 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267.

    Article  CAS  PubMed  Google Scholar 

  • Ketmaier, V. & P. G. Bianco, 2015. Understanding and conserving genetic diversity in a world dominated by alien introductions and native transfers: the case study of primary and peripheral freshwater fishes in southern Europe. In Closs, G. P., M. Krkosek & J. D. Olden (eds), Conservation of Freshwater Fishes. Cambridge University Press, Cambridge: 506–534.

    Google Scholar 

  • Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fish. Kottelat, Freyhof, Cornol and Berlin.

    Google Scholar 

  • Laikre, L., L. M. Miller, A. Palmé, S. Palm, A. R. Kapuscinski, G. Thoresson & N. Ryman, 2005. Spatial genetic structure of northern pike (Esox lucius) in the Baltic Sea. Molecular Ecology 14: 1955–1964.

    Article  CAS  PubMed  Google Scholar 

  • Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson & D. G. Higgins, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  • Larsen, P. F., M. M. Hansen, E. E. Nielsen, L. F. Jensen & V. Loeschcke, 2005. Stocking impact and temporal stability of genetic composition in a brackish northern pike population (Esox lucius L.), assessed using microsatellite DNA analysis of historical and contemporary samples. Heredity 95: 136–143.

    Article  CAS  PubMed  Google Scholar 

  • Launey, S., F. Krieg, J. Morin & J. Laroche, 2003. Five new microsatellite markers for northern pike (Esox lucius). Molecular Ecology Notes 3: 366–368.

    Article  CAS  Google Scholar 

  • Launey, S., J. Morin, S. Minery & J. Laroche, 2006. Microsatellite genetic variation reveals extensive introgression between wild and introduced stocks, and a new evolutionary unit in French pike Esox lucius L. Journal of Fish Biology 68: 193–216.

    Article  Google Scholar 

  • Lucentini, L., A. Palomba, L. Gigliarelli, H. Lancioni, M. Natali & F. Panara, 2006. Microsatellite polymorphism in Italian populations of northern pike (Esox lucius L.). Fisheries Research 80: 251–262.

    Article  Google Scholar 

  • Lucentini, L., A. Palomba, L. Gigliarelli, G. Sgaravizzi, H. Lancioni, L. Lanfaloni, M. Natali & F. Panara, 2009. Temporal changes and effective population size of an Italian isolated and supportive-breeding managed northern pike (Esox lucius) population. Fisheries Research 96: 139–147.

    Article  Google Scholar 

  • Lucentini, L., M. E. Puletti, C. Ricciolini, L. Gigliarelli, D. Fontaneto, L. Lanfaloni, F. Bilò, M. Natali & F. Panara, 2011. Molecular and phenotypic evidence of a new species of genus Esox (Esocidae, Esociformes, Actinopterygii): the Southern pike, Esox flaviae. PLoS ONE 6: e25218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maes, G. E., J. K. J. Van Houdt, D. De Charleroy & F. A. M. Volckaert, 2003. Indications for a recent Holarctic expansion of pike based on a preliminary study of mtDNA variation. Journal of Fish Biology 63: 254–259.

    Article  CAS  Google Scholar 

  • McKelvey, K. S., M. K. Young, T. M. Wilcox, D. M. Bingham, K. L. Pilgrim & M. K. Schwartz, 2016. Patterns of hybridization among cutthroat trout and rainbow trout in northern Rocky Mountain streams. Ecology and Evolution 6: 688–706.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meraner, A., A. Venturi, G. F. Ficetola, S. Rossi, A. Candiotto & A. Gandolfi, 2013a. Massive invasion of exotic Barbus barbus and introgressive hybridization with endemic Barbus plebejus in Northern Italy: where, how and why? Molecular Ecology 22: 5295–5312.

    Article  CAS  PubMed  Google Scholar 

  • Meraner, A., G. Unfer & A. Gandolfi, 2013b. Good news for conservation: limited genetic signatures of inter-basin fish transfer in Thymallus thymallus (Salmonidae) from the Upper Drava River. Knowledge and Management of Aquatic Ecosystems 409: 1–17.

    Article  Google Scholar 

  • Meraner, A., P. Gratton, F. Baraldi & A. Gandolfi, 2013c. Nothing but a trace left? Autochthony and conservation status of Northern Adriatic Salmo trutta inferred from PCR multiplexing, mtDNA control region sequencing and microsatellite analysis. Hydrobiologia 702: 201–213.

    Article  CAS  Google Scholar 

  • Meraner, A., L. Cornetti & A. Gandolfi, 2014. Defining conservation units in a stocking-induced genetic melting pot: unraveling native and multiple exotic genetic imprints of recent and historical secondary contact in Adriatic grayling. Ecology and Evolution 4: 1313–1327.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller, L. M. & A. R. Kapuscinski, 1997. Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 147: 1249–1258.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller, L. M. & W. Senanan, 2003. A review of northern pike population genetics research and its implications for management. North American Journal of Fisheries Management 23: 297–306.

    Article  Google Scholar 

  • Nicod, J.-C., Y. Z. Wang, L. Excoffier & C. R. Largiader, 2004. Low levels of mitochondrial DNA variation among central and southern European Esox lucius populations. Journal of Fish Biology 64: 1442–1449.

    Article  CAS  Google Scholar 

  • Pedreschi, D., M. Kelly-Quinn, J. Caffrey, M. O’Grady & S. Mariani, 2014. Genetic structure of pike (Esox lucius) reveals a complex and previously unrecognized colonization history of Ireland. Journal of Biogeography 41: 548–560.

    Article  PubMed  Google Scholar 

  • Pritchard, J., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts, D. G., C. A. Gray, R. J. West & D. J. Ayre, 2010. Marine genetic swamping: hybrids replace an obligately estuarine fish. Molecular Ecology 19: 508–520.

    Article  PubMed  Google Scholar 

  • Rondinini, C., A. Battistoni, V. Peronace & C. Teofili, 2013. Lista Rossa IUCN dei Vertebrati Italiani. Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Roma, pp. 54.

  • Seeb, J. E., L. W. Seeb, D. W. Oates & F. M. Utter, 1987. Genetic variation and postglacial dispersal of populations of northern pike (Esox lucius) in North America. Canadian Journal of Fisheries and Aquatic Sciences 44: 556–561.

    Article  Google Scholar 

  • Senanan, W. & R. Kapuscinski, 2000. Genetic relationships among populations of northern pike (Esox lucius). Canadian Journal of Fisheries and Aquatic Sciences 57: 391–404.

    Article  Google Scholar 

  • Skog, A., L. Vøllestad, N. Stenseth, A. Kasumyan & K. Jakobsen, 2014. Circumpolar phylogeography of the northern pike (Esox lucius) and its relationship to the Amur pike (E. reichertii). Frontiers in Zoology 11: 67.

    Article  Google Scholar 

  • Sloss, B. L., R. P. Franckowiak & E. L. Murphy, 2008. Development of new microsatellite loci and multiplex reactions for muskellunge (Esox masquinongy). Molecular Ecology Resources 8: 811–813.

    Article  CAS  PubMed  Google Scholar 

  • Smith, K. G. & W. R. T. Darwall, 2006. The status and distribution of freshwater fish endemic to the Mediterranean Basin. IUCN, Gland.

    Google Scholar 

  • Storey, J. D., 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society Series B 64: 479–498.

    Article  Google Scholar 

  • Sušnik Bajec, S., G. Pustovrh, D. Jesenšek & A. Snoj, 2015. Population genetic SNP analysis of marble and brown trout in a hybridization zone of the Adriatic watershed in Slovenia. Biological Conservation 184: 239–250.

    Article  Google Scholar 

  • Vähä, J. P. & C. R. Primmer, 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molecular Ecology 15: 63–72.

    Article  PubMed  Google Scholar 

  • Wang, J., C. Wang, L. Qian, Y. Ma, X. Yang, Z. Jeney & S. Li, 2011. Genetic characterization of 18 novel microsatellite loci in northern pike (Esox lucius L.). Genetics and Molecular Biology 34: 169–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, W. P., C. O. Ostberg, P. Keim & G. H. Thorgaard, 2001. Genetic characterization of hybridization and introgression between anadromous rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki). Molecular Ecology 10: 921–930.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Fisheries Offices (H. Erhard and H. Grund, Autonomous Provinces of Bolzano/Bozen; S. Filippini and R. Sala, Province of Lodi), researchers (E. Eschbach, Leibniz-Institute for Freshwater Ecology and Inland Fisheries, Department of Biology and Ecology of Fishes; T. Friedrich and G. Unfer, BOKU Vienna – University of Natural Resources and Life Sciences, Institute for Hydrobiology and Aquatic Ecosystem Management), free-lance ichthyologists (L. Betti; S. Rossi), professional fishermen (A. Andreis) and anglers (W. Arnoldo; Fisheries Association of Appiano/Eppan) who contributed to the collection of tissue samples.

Author information

Authors and Affiliations

  1. Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach (FEM), Via E. Mach 1, 38010, San Michele all’Adige, TN, Italy

    Andrea Gandolfi, Claudio Ferrari, Barbara Crestanello & Matteo Girardi

  2. Department of Life Sciences, University of Parma, Parco Area delle scienze 11/a, 43124, Parma, Italy

    Claudio Ferrari

  3. Department of Chemistry, Biology and Biotechnologies, University of Perugia, Via Elce di Sotto, 06123, Perugia, Italy

    Livia Lucentini

  4. Department of Forestry, Hunting and Fisheries Office of the Autonomous Province of Bolzano, Via Brennero 6, 39100, Bolzano, Italy

    Andreas Meraner

Authors
  1. Andrea Gandolfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudio Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Crestanello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matteo Girardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Livia Lucentini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andreas Meraner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Gandolfi.

Additional information

Handling editor: Christian Sturmbauer

An erratum to this article is available at http://dx.doi.org/10.1007/s10750-017-3250-z.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2016_3083_MOESM1_ESM.pdf

NewHybrids analysis on a simulated dataset including individuals of E. lucius, E. flaviae and different hybrid classes (F1, F2 and backcrosses to E. lucius and E. flaviae). Supplementary material 1 (PDF 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gandolfi, A., Ferrari, C., Crestanello, B. et al. Population genetics of pike, genus Esox (Actinopterygii, Esocidae), in Northern Italy: evidence for mosaic distribution of native, exotic and introgressed populations. Hydrobiologia 794, 73–92 (2017). https://doi.org/10.1007/s10750-016-3083-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-3083-1

Keywords

Search

Navigation