Two distinct evolutionary lineages of the Astacus leptodactylus species-complex (Decapoda : Astacidae) inferred by phylogenetic analyses
Ivana Maguire A D , Martina Podnar B , Mišel Jelić A , Anamaria Štambuk A , Anne Schrimpf C , Holger Schulz C and Goran Klobučar A
+ Author Affiliations
- Author Affiliations
A University of Zagreb, Faculty of Science, Department of Zoology, Rooseveltov trg 6, 10000 Zagreb, Croatia.
B Croatian Natural History Museum, Demeterova 1, 10000 Zagreb, Croatia.
C Universität Koblenz-Landau, Institute for Environmental Sciences, Fortstrasse 7, 76829 Landau, Germany.
D Corresponding author. Email: imaguire@zg.biol.pmf.hr
Invertebrate Systematics 28(2) 117-123 https://doi.org/10.1071/IS13030
Submitted: 11 June 2013 Accepted: 17 October 2013 Published: 30 May 2014
Abstract
Narrow-clawed crayfish (Astacus leptodactylus Eschscholtz, 1823 species-complex) is one of five European freshwater crayfish species. Even though widely distributed, it hasn’t been frequently studied and its taxonomy and systematics are unresolved. The results of a recent comparative morphometric character study revealed that morphometry of Asian and European populations differ significantly. In this research, for the first time, mitochondrial molecular markers (16S rRNA and COI) were used with the aim of elucidating the phylogenetic relationship between European and Asian populations of the narrow-clawed crayfish. Analyses included crayfish from Croatia, Bulgaria, Armenia, Russia, Poland and Turkey, and three different optimality criteria were applied. Phylogenetic relationships were reconstructed using the COI dataset, as well as the concatenated one (COI + 16S rRNA). For both datasets, congruent topologies were obtained and trees were characterised by the existence of two well supported phylogroups, one that included European populations, and the other Asian. Results indicate the presence of distinct evolutionary lineages within the A. leptodactylus species-complex, and corroborate previous results obtained using morphometric analyses.
References
Albrecht, H. (1982). Das System der europäischen Flußkrebse (Decapoda, Astacidae): Vorschlag und Begründung. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 79, 187–210.Albrecht, H. (1983). Besiedlungsgeschichte und ursprüngliche holozäne Verbreitung der europäischen Flusskrebse (Decapoda: Astacidae). Spixiana 6, 61–77.
Bij de Vaate, A., Jazdzewski, K., Ketelaars, H. A. M., Gollasch, S., and Van der Velde, G. (2002). Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59, 1159–1174.
| Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe.Crossref | GoogleScholarGoogle Scholar |
Bott, R. (1950). Die Flusskrebse Europas (Decapoda, Astacidae). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 483, 1–36.
Bott, R. (1972). Besiedlungsgeschichte und Systematik der Astaciden West-Europas unter besonderer Berücksichtigung der Schweiz. Revue Suisse de Zoologie 79, 397–408.
Brodski, S. Y. (1983). On the systematics of palaearctic crayfishes (Crustacea, Astacidae). Freshwater Crayfish 5, 464–469.
Cataudella, R., Paolucci, M., Delaunay, C., Ropiquet, A., Hassanin, A., and Balsamo, M. (2010). Genetic variability of Austropotamobius italicus in the Marches region: implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 20, 261–268.
| Genetic variability of Austropotamobius italicus in the Marches region: implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Farris, J. S., Källersjö, M., Kluge, A. G., and Bult, C. (1994). Testing significance of incongruence. Cladistics 10, 315–319.
| Testing significance of incongruence.Crossref | GoogleScholarGoogle Scholar |
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed |
Fourment, M., and Gibbs, M. J. (2006). PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evolutionary Biology 6, 1.
| PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change.Crossref | GoogleScholarGoogle Scholar | 16388682PubMed |
Fratini, S., Zaccara, S., Barbaresi, S., Grandjean, F., Souty-Grosset, C., and Crosa, G. (2005). Phylogeography of the threatened crayfish (genus Austropotamobius) in Italy: implications for its taxonomy and conservation. Heredity 94, 108–118.
| Phylogeography of the threatened crayfish (genus Austropotamobius) in Italy: implications for its taxonomy and conservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOnu7jL&md5=5ade70dc53256e8e180d35ca6debe950CAS | 15483655PubMed |
Grandjean, F., and Souty-Grosset, C. (1996). Isolation and characterization of mitochondrial DNA from the endangered white-clawed crayfish Austropotamobius pallipes pallipes, Lereboullet, 1858. Bulletin Francais de la Peche et de la Pisciculture 343, 175–182.
| Isolation and characterization of mitochondrial DNA from the endangered white-clawed crayfish Austropotamobius pallipes pallipes, Lereboullet, 1858.Crossref | GoogleScholarGoogle Scholar |
Grandjean, F., and Souty-Grosset, C. (2000). Mitochondrial DNA variation and population genetic structure of the white-clawed crayfish, Austropotamobius pallipes. Conservation Genetics 1, 309–319.
| Mitochondrial DNA variation and population genetic structure of the white-clawed crayfish, Austropotamobius pallipes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslSksbg%3D&md5=1a8a6256773f02328589c2b99ef070e0CAS |
Grandjean, F., Harris, D. J., Souty-Grosset, C., and Crandall, K. A. (2000). Systematics of the European endangered crayfish species Austropotamobius pallipes (Decapoda: Astacidae). Journal of Crustacean Biology 20, 522–529.
Grandjean, F., Bouchon, D., and Souty-Grosset, C. (2002a). Systematics of the European endangered crayfish species Austropotamobius pallipes pallipes (Decapoda: Astacidae) with a re-examination of Austropotamobius berndhauseri status. Journal of Crustacean Biology 22, 677–681.
Grandjean, F., Frelon-Raimond, M., and Souty-Grosset, C. (2002b). Compilation of molecular and morphological data for the phylogeny of in the genus Austropotamobius: one species or several? Bulletin Francais de la Peche et de la Pisciculture 367, 671–680.
| Compilation of molecular and morphological data for the phylogeny of in the genus Austropotamobius: one species or several?Crossref | GoogleScholarGoogle Scholar |
Grandjean, F., Gouin, N., Keith, P., Noël, P., Persat, H., Reynolds, J., Schulz, H., Smietana, P., and Souty-Grosset, C. (2006). Systematics and phylogeny of freshwater crayfish, with particular reference to historical biogeography of Europe. In ‘Atlas of Crayfish in Europe’. (Eds C. Souty-Grosset, D. M. Holdich, P. Y. Noël, J. D. Reynolds and P. Haffner.) pp. 11–23. (Museum national d’Histoire naturelle: Paris, France.)
Harlioğlu, M. (2004). The present situation of freshwater crayfish, Astacus leptodactylus (Eschscholtz, 1823) in Turkey. Aquaculture 230, 181–187.
| The present situation of freshwater crayfish, Astacus leptodactylus (Eschscholtz, 1823) in Turkey.Crossref | GoogleScholarGoogle Scholar |
Hewitt, G. M. (1999). Post-glacial recolonization of European biota. Biological Journal of the Linnean Society. Linnean Society of London 68, 87–112.
| Post-glacial recolonization of European biota.Crossref | GoogleScholarGoogle Scholar |
Holdich, D. M., Haffner, P., and Noël, P. (2006). Species files. In ‘Atlas of Crayfish in Europe’. (Eds C. Souty-Grosset, D. M. Holdich, P. Noël, J. D. Reynolds and P. Haffner.) pp. 56–131. (Museum national d’Histoire naturelle: Paris, France.)
Holdich, D. M., Reynolds, J. D., Souty-Grosset, C., and Sibley, P. J. (2009). A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems 394–395, 11.
| A review of the ever increasing threat to European crayfish from non-indigenous crayfish species.Crossref | GoogleScholarGoogle Scholar |
Karaman, M. S. (1962). Ein Beitrag zur Systematik der Astacidae (Decapoda). Crustaceana 3, 173–191.
| Ein Beitrag zur Systematik der Astacidae (Decapoda).Crossref | GoogleScholarGoogle Scholar |
Karaman, M. S. (1963). Studie der Astacidae (Crustacea, Decapoda). II Teil. Hydrobiologia 22, 111–132.
| Studie der Astacidae (Crustacea, Decapoda). II Teil.Crossref | GoogleScholarGoogle Scholar |
Klobučar, G., Podnar, M., Jelić, M., Franjević, D., Faller, M., Štambuk, A., Gottstein, S., Simić, V., and Maguire, I. (2013). Role of the Dinaric Karst (western Balkans) in shaping the phylogeographic structure of the threatened crayfish Austropotamobius torrentium. Freshwater Biology 58, 1089–1105.
| Role of the Dinaric Karst (western Balkans) in shaping the phylogeographic structure of the threatened crayfish Austropotamobius torrentium.Crossref | GoogleScholarGoogle Scholar |
Kouba, A., Buřič, M., and Petrusek, A. (2013). Druhy raků v Evropĕ. In ‘Biologie a chov raků’. (Ed. P. Kozák.) pp. 75–153. (Jihočeská univerzita v Českých Budějovicích: Vodňany, Czech Republic.)
Largiadèr, C. R., Herger, F., Lörtscher, M., and Scholl, A. (2000). Assessment of natural and artificial propagation of the white-clawed crayfish Austropotamobius pallipes species complex) in the Alpine region with nuclear and mitochondrial markers. Molecular Ecology 9, 25–37.
| Assessment of natural and artificial propagation of the white-clawed crayfish Austropotamobius pallipes species complex) in the Alpine region with nuclear and mitochondrial markers.Crossref | GoogleScholarGoogle Scholar | 10652073PubMed |
Lefébure, T., Douady, C. J., Gouy, M., and Gibert, J. (2006). Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.
| Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation.Crossref | GoogleScholarGoogle Scholar | 16647275PubMed |
Maguire, I., and Dakić, L. (2011). Comparative analyses of Astacus leptodactylus morphological characteristics from Croatia and Armenia. Biologia 66, 491–498.
| Comparative analyses of Astacus leptodactylus morphological characteristics from Croatia and Armenia.Crossref | GoogleScholarGoogle Scholar |
Maguire, I., Jelić, M., and Klobučar, G. (2011). Update on the distribution of freshwater crayfish in Croatia. Knowledge and Management of Aquatic Ecosystems 401, 31.
| Update on the distribution of freshwater crayfish in Croatia.Crossref | GoogleScholarGoogle Scholar |
Pedraza-Lara, C., Alda, F., Carranzy, S., and Doadrio, I. (2010). Mitochondrial DNA structure of the Iberian populations of the white-clawed crayfish, Austropotamobius italicus italicus (Faxon, 1914). Molecular Phylogenetics and Evolution 57, 327–342.
| Mitochondrial DNA structure of the Iberian populations of the white-clawed crayfish, Austropotamobius italicus italicus (Faxon, 1914).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqsL3O&md5=4a1f524944c7bba5e93eaffe11fd9a56CAS | 20601016PubMed |
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: Phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=a227fa0ae4120a3a8c06cab96986f12aCAS | 18397919PubMed |
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=d5b84f5cc16cfb75b367ced57a76cb2cCAS | 12912839PubMed |
Schubart, C. D., and Huber, M. G. J. (2006). Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin Francais de la Peche et de la Pisciculture 380–381, 1019–1028.
| Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae).Crossref | GoogleScholarGoogle Scholar |
Schulz, H. K., and Grandjean, F. (2005). Phylogeny of European crayfish – improving the taxonomy of European crayfish for a better conservation. Bulletin Francais de la Peche et de la Pisciculture 376–377, 829–836.
| Phylogeny of European crayfish – improving the taxonomy of European crayfish for a better conservation.Crossref | GoogleScholarGoogle Scholar |
Simon, C., Frat, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=d5c73c20640b01d4cb1718c8d993d994CAS |
Śmietana, P., Schulz, H. K., Keszka, S., and Schulz, R. (2006). A proposal for accepting Pontastacus as a genus of European crayfish within the family Astacidae based on a revision of the West and East European taxonomic literature. Bulletin Francais de la Peche et de la Pisciculture 380–381, 1041–1052.
| A proposal for accepting Pontastacus as a genus of European crayfish within the family Astacidae based on a revision of the West and East European taxonomic literature.Crossref | GoogleScholarGoogle Scholar |
Starobogatov, Y. I. (1995). Taxonomy and geographical distribution of crayfishes of Asia and East Europe (Crustacea, Decapoda, Astacoidei). Arthropoda Selecta 4, 3–25.
Stucki, T. P. (1999). Life cycle and life history of Astacus leptodactylus in Chatzensee Pond (Zurich) and Lake Ageri, Switzerland. Freshwater Crayfish 12, 430–448.
Swofford, D. L. (2001). ‘PAUP*: Phylogenetic Analysis using Parsimony (and other Methods).’ Version 4.0. beta10. (Sinauer Associates: Sunderland, MA.)
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=5ee5a71f721d24a7782516dc0ff5fcfcCAS | 21546353PubMed |
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=bae90a644b4721e65024ca4da74018baCAS | 7984417PubMed |
Trontelj, P., Machino, Y., and Sket, B. (2005). Phylogenetic and phylogeographic relationships in the crayfish genus Austropotamobius inferred from mitochondrial COI gene sequences. Molecular Phylogenetics and Evolution 34, 212–226.
| Phylogenetic and phylogeographic relationships in the crayfish genus Austropotamobius inferred from mitochondrial COI gene sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaqsbzJ&md5=5bfc35f2b8a216a26c3639a71537c39dCAS | 15579394PubMed |
Zaccara, S., Stefani, F., Galli, P., Nardi, P. A., and Crosa, G. (2004). Taxonomic implications in conservation management of white-clawed crayfish (Austropotamobius pallipes) (Decapoda, Astacidae) in Northern Italy. Biological Conservation 120, 1–10.
| Taxonomic implications in conservation management of white-clawed crayfish (Austropotamobius pallipes) (Decapoda, Astacidae) in Northern Italy.Crossref | GoogleScholarGoogle Scholar |
Zaccara, S., Stefani, F., and Crosa, G. (2005). Diversity of mitochondrial DNA of the endangered white-clawed crayfish (Austropotamobius italicus) in the Po River catchment. Freshwater Biology 50, 1262–1272.
| Diversity of mitochondrial DNA of the endangered white-clawed crayfish (Austropotamobius italicus) in the Po River catchment.Crossref | GoogleScholarGoogle Scholar |
Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. Thesis, University of Texas at Austin, TX, USA.
