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Genetic data on endangered twaite shad (Clupeidae) assessed in landlocked and anadromous populations: one or more species?

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Abstract

Seven Italian populations of twaite shad Alosa fallax from Northern and Central Italy were investigated to assess genetic diversity by Cytochrome b (Cytb) gene sequencing. The two ecotypes historically referred to landlocked and anadromous populations were investigated for the first time from a genetic point of view, to clarify their phylogenetic relationships. Moreover, results obtained from populations coming from separated Adriatic and Tyrrhenian basins were compared with data assessed in samples of allis shad Alosa alosa from the Atlantic basin. All the Italian samples were recognized at species level as A. fallax, differing for five mutations from A. alosa. The analyses confirmed the occurrence of a single phylogenetic lineage and of a single species within Italian waters, in both landlocked and migratory populations. The minimum spanning network identified six haplotypes for A. fallax and two haplotypes for A. alosa. The neighbour-joining tree and the maximum likelihood on the Cytb gene sequences confirmed two distinct lineages for A. alosa and A. fallax, without evidence of a separation at specific level within the A. fallax group. A weak separation due to incipient population differentiation was detected between anadromous and landlocked Italian populations, supporting the idea of a recent separation. The molecular data herein collected do not support the existence of the already controversial incipient species Alosa agone. Despite this, the two ecotypes could be considered as different management units from a conservation viewpoint.

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References

  • Alexandrino PJ, Ferrand N, Rocha J (1996) Genetic polymorphism of a hemoglobin chain and adenosine deaminase in European shads: evidence for the existence of two distinct genetic entities with natural hybridization. J Fish Biol 48:447–456

    Article  CAS  Google Scholar 

  • Alexandrino P, Faria R, Linhares D, Castro F, Le Corre M, Sabatiè R, Baglinière JL, Weiss S (2006) Interspecific differentiation and intraspecific substructure in two closely related clupeids with extensive hybridization, Alosa alosa and Alosa fallax. J Fish Biol 69:242–259

    Article  CAS  Google Scholar 

  • Andree KB, Angel Lopéz M, Alexandrino P, Faria R, Gisbert E (2011) A preliminary genetic analysis of a recently rediscovered population of the Twaite shad (Alosa fallax) in the Ebro river, Spain (Western Mediterranean). J Appl Ichthyol 27:21–23

    Article  Google Scholar 

  • Aprahamian MW, Baglinière JL, Sabatié R, Alexandrino P, Aprahamian CD (2002) Alosa alosa and Alosa fallax spp. Environment Agency, Bristol

    Google Scholar 

  • Baglinière JL (2000) Le genere Alosa sp. In: Baglinière JL, Elie P (eds) Les aloses Alosa alosa et Alosa fallax spp. INRA-Cemagref, Paris, pp 1–30

  • Bentzen P, Leggett WC, Brown GG (1993) Genetic relationships among the shads (Alosa) revealed by mitochondrial DNA analysis. J Fish Biol 43:909–917

    Article  CAS  Google Scholar 

  • Berti R, Paglianti A, Gherardi F, Gandolfi G, Tagliavini J (2006) Caratterizzazione di alose con marcatori molecolari. Biol Amb 20:253–257

    Google Scholar 

  • Bianco P (2002) The status of the twaite shad, Alosa agone, in Italy and the Western Balkans. Mar Ecol 23:51–64

    Article  Google Scholar 

  • Boisneau P, Mennesson-Boisneau C, Guyomard R (1992) Electrophoretic identity between allis shad Alosa alosa L. and twaite shad, Alosa fallax (Lacépède). J Fish Biol 40:731–738

    Article  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Coscia I, Rountree V, King JJ, Roche WK, Mariani S (2010) A highly permeable species boundary between two anadromous fishes. J Fish Biol 77:1137–1149

    Article  CAS  PubMed  Google Scholar 

  • Faria R, Wallner B, Weiss S, Alexandrino P (2004) Isolation and characterization of eight di nucleotide microsatellite loci from two closely related clupeid species (Alosa alosa and A. fallax). Mol Ecol Notes 4:586–588

    Article  CAS  Google Scholar 

  • Faria R, Weiss S, Alexandrino P (2006) Molecular phylogenetic perspective on the evolutionary history of Alosa spp. (Clupeidae). Mol Phylogenet Evol 40:298–304

    Article  CAS  PubMed  Google Scholar 

  • Faria R, Pinheiro A, Gabaldon T, Weiss S, Alexandrino P (2011) Molecular tools for species discrimination and detection of hybridization between two closely related Clupeid fishes Alosa alosa and A. fallax. J Appl Ichthyol 27:16–20

    Article  Google Scholar 

  • Faria R, Weiss S, Alexandrino P (2012) Comparative phylogeography and demographic history of European shads (Alosa alosa and A. fallax) inferred from mitochondrial DNA. BMC Evol Biol 12:194–214

    Article  PubMed Central  PubMed  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Article  CAS  PubMed  Google Scholar 

  • Freyhof J, Kottelat M (2008) Alosa fallax. In: IUCN 2011. IUCN red list of threatened species. Version 2011.2. http://www.iucnredlist.org. Accessed 1 Nov 2013

  • Freyhof J, Kottelat M (2010) Alosa alosa. In: IUCN 2011. IUCN red list of threatened species. Version 2011.2. http://www.iucnredlist.org. Accessed 1 Nov 2013

  • Gandolfi G, Zerunian S, Torricelli P, Marconato E (1991) I pesci delle acque interne italiane. Ministero dell’Ambiente-Servizio Conservazione Natura, Unione Zoologica Italiana e Istituto Poligrafico e Zecca dello Stato, Roma

    Google Scholar 

  • Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695

    Article  CAS  PubMed  Google Scholar 

  • Jolly MT, Maitland PS, Genner MJ (2011) Genetic monitoring of two decades of hybridization between allis shad (Alosa alosa) and twaite shad (Alosa fallax). Conserv Genet 12:1087–1100

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Jolly MT, Aprahamian MW, Hawkins SJ, Henderson PA, Hillman R, O’Maoiléidigh N, Maitland PS, Piper R, Genner MJ (2012) Population genetic structure of protected allis shad (Alosa alosa) and twaite shad (Alosa fallax). Mar Biol 159:675–687

    Article  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol

    Google Scholar 

  • Le Corre M, Alexandrino P, Sabatie MR, Aprahamian MW, Bagliniere JL (2005) Genetic characterisation of the Rhodanian twaite shad, Alosa fallax rhodanensis. Fish Manag Ecol 12:275–282

    Article  Google Scholar 

  • Lochet A, Boutry S, Rochard E (2009) Estuarine phase during seaward migration for allis shad Alosa alosa and twaite shad Alosa fallax future spawners. Ecol Freshw Fish 18:323–335

    Article  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics III. Genic homozygosity in populations which experience periodic bottlenecks. Genetics 111(3):691–703

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Rondinini C, Battistoni A, Peronace V, Teofili C (2013) Lista Rossa IUCN dei Vertebrati Italiani. pp 53, Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Rome

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Salviani I (1554) I Pesci. In Aquatilium animalium historiae. Edizioni Colombo Ristampe. Rome

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285

    CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taverny C, Belaud A, Elie P, Sabatié MR (2000) Influence des activités humaines. In: Les aloses Alosa alosa et Alosa fallax spp. J. L. Baglinière and P. Elie (eds). Inra-Cemagref, Paris, France, pp 227–248

  • Volk J, Bekkevold D, Loeschcke V (2007) Weak population differentiation in northern European populations of the endangered anadromous clupeid Alosa fallax. J Fish Biol 7:461–469

    Article  Google Scholar 

  • Whitehead PJP (1984) Clupeidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of north-eastern Atlantic and the Mediterranean, vol I. UNESCO, Paris

    Google Scholar 

  • Whitehead PJP (1985) FAO species catalogue, vol. 7. Clupeid fishes of the world (Suborder Clupeiodei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies, and wolf-herrings. Part I. FAO Fisheries Synopsis 125:1–303

    Google Scholar 

  • Zerunian S (2002) Condannati all’estinzione? Biodiversità, biologia, minacce e strategie di conservazione dei Pesci d’acqua dolce indigeni in Italia”. Edagricole, Bologna (Italy). (in Italian)

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Acknowledgments

All experimental procedures have been carried out in accordance to the Italian National Law on Animal Welfare. In particular, tissue sampling (small fin clip) has been collected during the narcosis status following electrofishing. Electrofishing activities have been authorized by local Authorities (Provinces and Regional Governments) and performed by patented technicians. No ethics approval number has been requested by the University of Parma, where the Research has been carried out. The authors would like to thank the Province of Grosseto, particularly Dr. Simona Piccini for supporting activities and project financing; Loris Ferrari for help with collecting samples from Como and Garda Lake and Taro River. Authors would also like to thank Dr. David Clavé from Association Migado Mairie, Rue Du Dr. Daude Lagrave 24520 Mouleydier (France) for A. alosa samples of Garonne River, and Dr. Immaculada Llorentz Gumbau for support in laboratory procedures.

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Correspondence to Francesco Nonnis Marzano.

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Chiesa, S., Piccinini, A., Lucentini, L. et al. Genetic data on endangered twaite shad (Clupeidae) assessed in landlocked and anadromous populations: one or more species?. Rev Fish Biol Fisheries 24, 659–670 (2014). https://doi.org/10.1007/s11160-014-9352-z

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