Complexity of biogeographic pattern in the endangered crayfish Austropotamobius italicus in northern Italy: molecular insights of conservation concern
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Abstract
The protection of freshwater biodiversity has become a priority task for conservation practices, as freshwater ecosystems host high levels of cryptic diversity, while also record similarly high rates of extinction. The Italian white-clawed crayfish Austropotamobius italicus is an endemic freshwater crustacean, threatened by several anthropogenic impacts such as habitat fragmentation, pollution, invasion of exotics, and climate change. Previous phylogenetic studies conducted in Italy pointed out a complex phylogeographic framework for the species, with four different subspecies currently recognized. Conservation efforts, particularly when involving restocking and reintroduction, require a detailed knowledge of their population genetics. In this study we describe the genetic structure of A. italicus populations in northern Italy (Lombardy Alpine foothills and northern Apennines) by using the informative mitochondrial marker cytochrome c oxidase subunit I, in order to assess their current evolutionary diversity and past phylogeographic history from a conservation perspective. Our results contribute to the mapping of the contact area among A. i. carsicus and A. i. carinthiacus in the Orobie Larian Prealps. More interestingly, we highlight the existence of two deeply differentiated evolutionary lineages within A. i. carsicus, showing alternative phylogeographic patterns and past demographic trends. We propose to consider these two clades as distinct molecular operational taxonomic units for the conservation of this endangered crayfish.
Keywords
COI mtDNA Phylogeography Alps Apennines Austropotamobius pallipes complex MOTUNotes
Acknowledgments
This study was partially supported by European Funds, through the Financial Instrument for the Environment (Life + 08 NAT/IT/000352—CRAINat), by ERSAF - Lombardia, by Fondazione Cariplo and Parco Adda Nord to D.G. and G.F.; and by the Italian Ministero Università e Ricerca (PRIN 2008) to P.G. We are grateful to T. Pagliani and F. Piccoli for providing the samples of A. i. meridionalis used to assess the phylogeny, and to the entire staff involved in the Life CRAINat project. Many thanks to E. Mazzarello for his valuable help to the lab work. Moreover, we thank three anonymous reviewers for their valuable comments.
Supplementary material
References
- Abramovitz JN (1996) Imperiled waters, impoverished future: the decline of freshwater ecosystems, vol 12. Worldwatch Paper, Worldwatch Institute, WashingtonGoogle Scholar
- Alderman DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Rev Sci et Tech—Off Int des épizoot 15:603–632Google Scholar
- Apte S, Smith PJ, Wallis GP (2007) Mitochondrial phylogeography of New Zealand freshwater crayfishes, Paranephrops spp. Mol Ecol 16:1897–1908. doi: 10.1111/j.1365-294X.2007.03224.x PubMedCrossRefGoogle Scholar
- Aquiloni L, Tricarico E, Gherardi F (2010) Crayfish in Italy: distribution, threats and management. Int Aquat Res 2:1–14Google Scholar
- Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
- Baker AM, Williams SA, Hughes JM (2003) Patterns of spatial genetic structuring in a hydropsychid caddisfly (Cheumatopsyche sp. AV1) from southeastern Australia. Mol Ecol 12:3313–3324. doi: 10.1046/j.1365-294X.2003.02011.x PubMedCrossRefGoogle Scholar
- Baker AM, Hughes JM, Dean JC, Bunn SE (2004) Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages. Mar Freshw Res 55:629–640. doi: 10.1071/MF04050 CrossRefGoogle Scholar
- Balian EV, Segers H, Lévèque C, Martens K (2008) The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595:627–637. doi: 10.1007/s10750-007-9246-3 CrossRefGoogle Scholar
- Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
- Bentley AI, Schmidt DJ, Hughes JM (2010) Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot. Freshw Biol 55:1861–1873. doi: 10.1111/j.1365-2427.2010.02420.x CrossRefGoogle Scholar
- Bertocchi S, Brusconi S, Gherardi F, Grandjean F, Souty-Grosset C (2008) Genetic variability of the threatened crayfish Austropotamobius italicus in Tuscany (Italy): implications for its management. Fundam Appl Limnol 173:153–164. doi: 10.1127/1863-9135/2008/0173-0153 CrossRefGoogle Scholar
- Brito D (2004) Lack of adequate taxonomic knowledge may hinder endemic mammal conservation in the Brazilian Atlantic forest. Biodivers Conserv 13:2135–2144. doi: 10.1023/B:BIOC.0000040005.89375.c0 CrossRefGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
- Cassens I, Van Waerebeek K, Best PB, Crespo EA, Reyes J, Milinkovitch MC (2003) The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Mol Ecol 12:1781–1792. doi: 10.1046/j.1365-294X.2003.01876.x PubMedCrossRefGoogle Scholar
- Changeux T (2003) Évolution de la répartition des écrevisses en France métropolitaine selon les enquêtes nationales menées par le conseil supérieur de la pêche de 1977 à 2001. Bull Français de la Pêche et de la Piscicolture 370–371:15–41. doi: 10.1051/kmae:2003002 CrossRefGoogle Scholar
- Chenoweth SF, Hughes JM (2003) Speciation and phylogeography in Caridina indistincta, a complex of freshwater shrimps from Australian heathland streams. Mar Freshw Res 54:807–812. doi: 10.1071/MF02168 CrossRefGoogle Scholar
- Chiesa S, Scalici M, Negrini R, Gibertini G, Nonnis Marzano F (2011) Fine-scale genetic structure, phylogeny and systematics of threatened crayfish species complex. Mol Phylogenet Evol 61:1–11. doi: 10.1016/j.ympev.2011.03.031 PubMedCrossRefGoogle Scholar
- Cook BD, Baker AM, Page TJ, Grant SC, Fawcett JH, Hurwood DA, Hughes JM (2006) Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification. Mol Ecol 15:1083–1093. doi: 10.1111/j.1365-294X.2006.02852.x PubMedCrossRefGoogle Scholar
- Cook BD, Page TJ, Hughes JM (2008) Importance of cryptic species for identifying ‘representative’ units of biodiversity for freshwater conservation. Biol Conserv 141:2821–2831. doi: 10.1016/j.biocon.2008.08.018 CrossRefGoogle Scholar
- Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
- Dawkins KL, Furse JM, Wild CH, Hughes JM (2010) Distribution and population genetics of the threatened freshwater crayfish genus Tenuibranchiurus (Decapoda: Parastacidae). Mar Freshw Res 61:1048–1055. doi: 10.1071/MF09294 CrossRefGoogle Scholar
- Diéguez-Uribeondo J, Royo F, Souty-Grosset C, Ropiquet A, Grandjean F (2008) Low genetic variability of the white-clawed crayfish in the Iberian Peninsula: its origin and management implications. Aquat Conserv Mar Freshw Ecosyst 18:19–31. doi: 10.1002/aqc.811 CrossRefGoogle Scholar
- Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182. doi: 10.1017/S1464793105006950 PubMedCrossRefGoogle Scholar
- Edmands S (2002) Does parental divergence predict reproductive compatibility? Trends Ecol Evol 17:520–527. doi: 10.1016/S0169-5347(02)02585-5 CrossRefGoogle Scholar
- Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
- Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50Google Scholar
- Filipová L, Holdich DM, Lesobre J, Grandjean F, Petrusek A (2010) Cryptic diversity within the invasive virile crayfish Orconectes virilis (Hagen 1870) species complex: new lineages recorded in both native and introduced ranges. Biol Invasions 12:983–989. doi: 10.1007/s10530-009-9526-0 CrossRefGoogle Scholar
- Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850. doi: 10.1046/j.1365-294X.2002.01485.x PubMedCrossRefGoogle Scholar
- Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedCrossRefGoogle Scholar
- Fratini S, Zaccara S, Barbaresi S, Grandjean F, Souty-Grosset C, Crosa G, Gherardi F (2005) Phylogeography of the threatened crayfish (genus Austropotamobius) in Italy: implications for its taxonomy and conservation. Heredity 94:108–118. doi: 10.1038/sj.hdy.6800581 PubMedCrossRefGoogle Scholar
- Füreder L, Gherardi F, Holdich DM, Reynolds J, Sibley PJ, Southy-Grosset C (2010) Austropotamobius pallipes. The IUCN Red List of Threatened Species. Version 2014.2. http://www.iucnredlist.org. Accessed 22 Oct 2014
- Galeotti P, Bernini G, Locatello L, Sacchi R, Rubolini D, Fasola M (2012) Sperm traits negatively covaries with size and asymmetry of a secondary sexual trait in a freshwater crayfish. PLOS One 7:e43771. doi: 10.1371/journalpone.0043771 PubMedPubMedCentralCrossRefGoogle Scholar
- Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshw Behav Physiol 39:175–191. doi: 10.1080/10236240600869702 CrossRefGoogle Scholar
- Gherardi F, Coignet A, Souty-Grosset C, Spigoli D, Aquiloni L (2013) Climate warming and the agonistic behaviour of invasive crayfishes in Europe. Freshw Biol 58:1958–1967. doi: 10.1111/fwb.12183 CrossRefGoogle Scholar
- Ghia D, Fea G, Sacchi R, Di Renzo G, Garozzo P, Marrone M, Piccoli F, Porfirio S, Santillo D, Salvatore B, Scoccia M, Di Francesco M, Fracassi G, Comini B, Pagliani T, Nardi PA (2013) Modelling environmental niche for the endangered crayfish Austropotamobius pallipes complex in northern and central Italy. Freshw Crayfish 19:189–195. doi: 10.5869/fc.2013.v19-2.189 Google Scholar
- Gouin N, Grandjean F, Pain S, Souty-Grosset C, Reynolds JD (2003) Origin and colonization history of the white-clawed crayfish, Austropotamobius pallipes, in Ireland. Heredity 91:70–77. doi: 10.1038/sj.hdy.6800282 PubMedCrossRefGoogle Scholar
- Gouin N, Grandjean F, Souty-Grosset C (2006) Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications. Freshw Biol 51:1369–1387. doi: 10.1111/j.1365-2427.2006.01570.x CrossRefGoogle Scholar
- Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
- Haye PA, Kornfield I, Watling L (2004) Molecular insights into Cumacean family relationships (Crustacea, Cumacea). Mol Phylogenet Evol 30:798–809. doi: 10.1016/j.ympev.2003.08.003 PubMedCrossRefGoogle Scholar
- Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. doi: 10.1111/j.1095-8312.1996.tb01434.x CrossRefGoogle Scholar
- Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi: 10.1038/35016000 PubMedCrossRefGoogle Scholar
- Holdich DM, Reynolds DJ, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 394–395:11. doi: 10.1051/kmae/2009025 CrossRefGoogle Scholar
- Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913. doi: 10.1080/10635150490522629 PubMedCrossRefGoogle Scholar
- Jenkins M (2003) Prospects for biodiversity. Science 302:1175–1177. doi: 10.1126/science.1088666 PubMedCrossRefGoogle Scholar
- Klobučar GIV, Podnar M, Jelić M, Franjević D, Faller M, Štambuk A, Gottstein S, Simić V, Maguire I (2013) Role of the Dinaric Karst (western Balkans) in shaping the phylogeographic structure of the threatened crayfish Austropotamobius torrentium. Freshw Biol 58:1089–1105. doi: 10.1111/fwb.12110 CrossRefGoogle Scholar
- Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi: 10.1093/bioinformatics/btp187 PubMedCrossRefGoogle Scholar
- Malmqvist B, Rundle S (2002) Threats to the running water ecosystems of the world. Environ Conserv 29:134–153. doi: 10.1017/S0376892902000097 CrossRefGoogle Scholar
- Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253. doi: 10.1038/35012251 PubMedCrossRefGoogle Scholar
- Martinuzzi S, Januchowski-Hartley SR, Pracheil BM, McIntyre PB, Plantinga AJ, Lewis DJ, Radeloff VC (2014) Threats and opportunities for freshwater conservation under future land use change scenarios in the United States. Glob Change Biol 20:113–124. doi: 10.1111/gcb.12383 CrossRefGoogle Scholar
- Mathews LM, Adams L, Anderson E, Basile M, Gottardi E, Buckholt MA (2008) Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex. Mol Phylogenet Evol 48:126–135. doi: 10.1016/j.ympev.2008.02.006 PubMedCrossRefGoogle Scholar
- McAllister DE, Hamilton AL, Harvey BJ (1997) Global freshwater biodiversity: striving for the integrity of freshwater ecosystems. Sea wind: bulletin of Ocean Voice International. Ocean Voice International, OttawaGoogle Scholar
- Meyran JC, Taberlet P (1998) Mitochondrial DNA polymorphism among alpine populations of Gammarus lacustris (Crustacea, Amphipoda). Freshw Biol 39:259–265. doi: 10.1046/j.1365-2427.1998.00277.x CrossRefGoogle Scholar
- Meyran J-C, Monnerot M, Taberlet P (1997) Taxonomic status and phylogenetic relationships of some species of the genus Gammarus (Crustacea, Amphipoda) deduced from mitochondrial DNA sequences. Mol Phylogenet Evol 8:1–10. doi: 10.1006/mpev.1996.0399 PubMedCrossRefGoogle Scholar
- Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375. doi: 10.1016/0169-5347(94)90057-4 PubMedCrossRefGoogle Scholar
- Moritz C, McGuigan K, Bernatchez L (2002) Conservation of freshwater fishes: integrating evolution and genetics with ecology. In: Collares-Pereira MJ, Cowx IG, Coelho MM (eds) Conservation of freshwater fishes: options for the future. Blackwell Science, Oxford, pp 293–310Google Scholar
- Morpurgo M, Aquiloni L, Bertocchi S, Brusconi S, Tricarico E, Gherardi F (2010) Distribuzione dei gamberi d’acqua dolce in Italia. Studi Trent Sci Nat 87:125–132Google Scholar
- Nardi PA, Bernini F, Bo T, Bonardi A, Fea G, Ghia D, Negri A, Razzetti E, Rossi S, Spairani M (2005) Status of Austropotamobius pallipes complex in the watercourses of the Alessandria province (N-W Italy). Bull Fr Peche Piscic 376–377:585–598. doi: 10.1051/kmae:2005017 CrossRefGoogle Scholar
- Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
- Ovenden JR, White RW (1990) Mitochondrial and allozyme genetics of incipient speciation in a landlocked population of Galaxias truttaceus (Pisces: Galaxiidae). Genetics 124:701–716PubMedPubMedCentralGoogle Scholar
- Page TJ, Hughes JM (2007) Phylogeographic structure in an Australian freshwater shrimp largely pre-dates the geological origins of its landscape. Heredity 98:222–231. doi: 10.1038/sj.hdy.6800932 PubMedCrossRefGoogle Scholar
- Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedCrossRefGoogle Scholar
- Perdices A, Sayanda D, Coelho MM (2005) Mitochondrial diversity of Opsariichthys bidens (Teleostei, Cyprinidae) in three Chinese drainages. Mol Phylogenet Evol 37:920–927. doi: 10.1016/j.ympev.2005.04.020 PubMedCrossRefGoogle Scholar
- Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. doi: 10.1093/molbev/msn083 PubMedCrossRefGoogle Scholar
- Rambaut A (2009) “FigTree version 1.3. 1.” Computer program distributed by the author, website: http://tree.bio.ed.ac.uk/software/figtree/ Accessed 4 Jan 2011
- Rambaut A, Drummond AJ (2007) Tracer v1. 4. http://beast.bio.ed.ac.uk/Tracer. Accessed 4 Jan 2011
- Revenga C, Mock G (2000) Freshwater biodiversity in crisis. Earth Trends World Resources Institute, pp 1–4Google Scholar
- Ricciardi A, Rasmussen JB (1999) Extinction rates of North American freshwater fauna. Conserv Biol 13:1220–1222. doi: 10.1046/j.1523-1739.1999.98380.x CrossRefGoogle Scholar
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi: 10.1093/sysbio/sys029 PubMedPubMedCentralCrossRefGoogle Scholar
- Rozen S, Skaletsky HJ (1998) Primer3. Code available at http://www-genome.wi.mit.edu/genome_software/other/primer3.html. Accessed 4 Jan 2011
- R Core Team (2014) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org/. Accessed 18 Nov 2014
- Saunders DL, Meeuwig JJ, Vincent ACJ (2002) Freshwater protected areas: strategies for conservation. Conserv Biol 16:30–41. doi: 10.1046/j.1523-1739.2002.99562.x CrossRefGoogle Scholar
- Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555. doi: 10.1111/j.1365-294X.2005.02683.x PubMedCrossRefGoogle Scholar
- Scotti I, Vendramin GG, Matteotti LS, Scarponi C, Sari-Gorla M, Binelli G (2000) Postglacial recolonization routes for Picea abies K. in Italy as suggested by the analysis of sequence-characterized amplified region (SCAR) markers. Mol Ecol 9:699–708. doi: 10.1046/j.1365-294x.2000.00911.x PubMedCrossRefGoogle Scholar
- Shull HC, Pérez-Losada M, Blair D, Sewell K, Sinclair EA, Lawler S, Ponniah M, Crandall KA (2005) Phylogeny and biogeography of the freshwater crayfish Euastacus (Decapoda: Parastacidae) based on nuclear and mitochondrial DNA. Mol Phylogenet Evol 37:249–263. doi: 10.1016/j.ympev.2005.04.034 PubMedCrossRefGoogle Scholar
- Silvestro D, Michalak I (2012) RaxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. doi: 10.1007/s13127-011-0056-0 CrossRefGoogle Scholar
- Souty-Grosset C, Reynolds JD (2009) Current ideas on methodological approaches in European crayfish conservation and restocking procedures. Knowl Manag Aquat Ecosyst 01:394–395. doi: 10.1051/kmae/2009021 Google Scholar
- Souty-Grosset C, Grandjean F, Raimond R, Frelon M, Debenest C, Bramard M (1997) Conservation genetics of the white-clawed crayfish Austropotamobius pallipes: the usefulness of the mitochondrial DNA marker. Bull Fr Peche Piscic 347:677–692. doi: 10.1051/kmae/1997055 CrossRefGoogle Scholar
- Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (eds) (2006) Atlas of Crayfish in Europe vol Patrimoines Naturels. Muséum national d’Histoire naturelle, ParisGoogle Scholar
- Stefani F, Zaccara S, Delmastro GB, Buscarino M (2011) The endangered white-clawed crayfish Austropotamobius pallipes (Decapoda, Astacidae) east and west of the Maritime Alps: a result of human translocation? Conserv Genet 12:51–60. doi: 10.1007/s10592-009-9986-x CrossRefGoogle Scholar
- Stefani F, Gentilli A, Sacchi R, Razzetti E, Pellitteri-Rosa D, Pupin F, Galli P (2012) Refugia within refugia as a key to disentangle the genetic pattern of a highly variable species: the case of Rana temporaria Linnaeus, 1758 (Anura, Ranidae). Mol Phylogenet Evol 65:718–726. doi: 10.1016/j.ympev.2012.07.022 PubMedCrossRefGoogle Scholar
- Stehlik I (2000) Nunataks and peripheral refugia for alpine plants during quaternary glaciation in the middle part of the Alps. Bot Helv 110:25–30. doi: 10.5169/seals-73583 Google Scholar
- Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180. doi: 10.1016/S0006-3207(98)00066-4 CrossRefGoogle Scholar
- Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29:344–358. doi: 10.1899/08-171.1 CrossRefGoogle Scholar
- Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464. doi: 10.1046/j.1365-294x.1998.00289.x PubMedCrossRefGoogle Scholar
- Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
- 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. doi: 10.1093/molbev/msr121 PubMedPubMedCentralCrossRefGoogle Scholar
- Trontelj P, Machino Y, Sket B (2005) Phylogenetic and phylogeographic relationships in the crayfish genus Austropotamobius inferred from mitochondrial COI gene sequences. Mol Phylogenet Evol 34:212–226. doi: 10.1016/j.ympev.2004.09.010 PubMedCrossRefGoogle Scholar
- Versteegen M, Lawler S (1997) Population genetics of the Murray river crayfish, Euastacus armatus. Freshw Crayfish 11:146–158Google Scholar
- Vorburger C, Ribi G (1999) Aggression and competition for shelter between a native and an introduced crayfish in Europe. Freshw Biol 42:111–119. doi: 10.1046/j.1365-2427.1999.00465.x CrossRefGoogle Scholar
- Wilcox TP, Zwickl DJ, Heath TA, Hillis DM (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol Phylogenet Evol 25:361–371. doi: 10.1016/S1055-7903(02)00244-0 PubMedCrossRefGoogle Scholar
- Witt JD, Threloff DL, Hebert PD (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Mol Ecol 15:3073–3082. doi: 10.1111/j.1365-294X.2006.02999.x PubMedCrossRefGoogle Scholar
- Wright S (1978) Evolution and the genetics of populations: variability within and among natural populations vol IV. Evolution and the genetics of populations: a treatise. University of Chicago Press, ChicagoGoogle Scholar
- Zaccara S, Stefani F, Crosa G (2005) Diversity of mitochondrial DNA of the endangered white-clawed crayfish (Austropotamobius italicus) in the Po River catchment. Freshw Biol 50:1262–1272. doi: 10.1111/j.1365-2427.2005.01385.x CrossRefGoogle Scholar