Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular systematics reveals multiple lineages and cryptic speciation in the freshwater crayfish Parastacus brasiliensis (von Martens, 1869) (Crustacea : Decapoda : Parastacidae)

Ivana Miranda https://orcid.org/0000-0002-8820-6681 A D E , Kelly M. Gomes B , Felipe B. Ribeiro B D , Paula B. Araujo B , Catherine Souty-Grosset C and Christoph D. Schubart D
+ Author Affiliations
- Author Affiliations

A Departamento de Biologia Aplicada, Invertebrate Morphology Laboratory, Aquaculture Center Universidade Estadual Paulista, Jaboticabal, SP, Brazil.

B Programa de Pós-Graduação em Biologia Animal, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.

C Laboratoire Ecologie & Biologie des Interactions, UMR CNRS 7267, Equipe Ecologie Evolution Symbiose, Université de Poitiers, Poitiers, France.

D Zoology and Evolutionary Biology, Universität Regensburg, Regensburg, Germany.

E Corresponding author. Email: yvanah@yahoo.com

Invertebrate Systematics 32(6) 1265-1281 https://doi.org/10.1071/IS18012
Submitted: 14 February 2018  Accepted: 8 June 2018   Published: 27 November 2018

Abstract

The characterisation of intraspecific genetic diversity in representatives of the South American crayfish genus Parastacus Huxley, 1879 is here carried out for the first time by comparing populations of Parastacus brasiliensis (von Martens, 1869) as currently defined. Phylogenetic reconstructions based on mitochondrial and nuclear markers indicate the existence of multiple lineages, of which only one can be considered as P. brasiliensis sensu stricto. In addition, there are seven other lineages, one of which is the subspecies Parastacus brasiliensis promatensis Fontoura & Conter, 2008, which is here elevated to species level. We thereby increase to 14 the number of recognised species within Parastacus in South America. Genetic distances among P. brasiliensis sensu stricto and the lineages ‘A’, ‘B’ and ‘C’ increase with geographical distances, suggesting isolation by distance as an important driver of diversification, and eventually speciation, in these burrowing crayfishes. Parastacus brasiliensis occurs mainly in the Guaíba Lake basin and studied populations show limited connectivity and gene flow, probably due to habitat fragmentation. On the basis of genetic and distribution data, the conservation status of P. brasiliensis sensu stricto is confirmed as Near Threatened (NT). These findings lead us to encourage the establishment of preservation areas for isolated populations. The importance of preserving the newly recognised distinct gene pools in order to maintain overall genetic diversity is emphasised.

Additional keywords: biodiversity, conservation, cryptic species, limnic ecosystems, multigenes.


References

Almerão, M. P., Rudolph, E., Souty-Grosset, C., Crandall, K. A., Buckup, L., Amouret, J., Verdi, A., Santos, S., and Araujo, P. B. (2015). The native South American crayfishes (Crustacea, Parastacidae): state of knowledge and conservation status. Aquatic Conservation 25, 288–301.
The native South American crayfishes (Crustacea, Parastacidae): state of knowledge and conservation status.Crossref | GoogleScholarGoogle Scholar |

Amos, W., and Harwood, J. (1998). Factors affecting levels of genetic diversity in natural populations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 177–186.
Factors affecting levels of genetic diversity in natural populations.Crossref | GoogleScholarGoogle Scholar |

ANA (2006). Topologia hídrica: método de construção e modelagem da base hidrográfica para suporte à gestão de recursos hídricos. Agência Nacional de Águas – Superintendência da Gestão de Informação, Brasília, Brazil.

Austin, C. M. A., Nguyen, T. T. T. A., Meewan, M. M. A., and Jerry, D. R. C. (2003). The taxonomy and phylogeny of the ‘Cherax destructor’ complex (Decapoda: Parastacidae) examined using mitochondrial 16S sequences. Australian Journal of Zoology 51, 99–110.
The taxonomy and phylogeny of the ‘Cherax destructor’ complex (Decapoda: Parastacidae) examined using mitochondrial 16S sequences.Crossref | GoogleScholarGoogle Scholar |

Avise, J. C. (2009). Phylogeography: retrospect and prospect. Journal of Biogeography 36, 3–15.
Phylogeography: retrospect and prospect.Crossref | GoogleScholarGoogle Scholar |

Baker, A. M., Hughes, J. M., Dean, J. C., and Bunn, S. E. (2004). Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages. Marine and Freshwater Research 55, 629–640.
Mitochondrial DNA reveals phylogenetic structuring and cryptic diversity in Australian freshwater macroinvertebrate assemblages.Crossref | GoogleScholarGoogle Scholar |

Baumart, J. S., Dalosto, M. M., Gonçalves, A. S., Palaoro, A. V., and Santos, S. (2015). How to deal with a bad neighbor? Strategies of sympatric freshwater decapods (Crustacea) for coexistence. Hydrobiologia 762, 29–39.
How to deal with a bad neighbor? Strategies of sympatric freshwater decapods (Crustacea) for coexistence.Crossref | GoogleScholarGoogle Scholar |

Bentley, A. I., Schmidt, D. J., and Hughes, J. M. (2010). Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot. Freshwater Biology 55, 1861–1873.
Extensive intraspecific genetic diversity of a freshwater crayfish in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |

Bertocchi, S., Brusconi, S., Gherardi, F., Grandjean, F., and Souty-Grosset, C. (2008). Genetic variability of the threatened crayfish Austropotamobius italicus in Tuscany (Italy): implications for its management. Fundamental and Applied Limnology; Official Journal of the International Association of Theoretical and Applied Limnology 173, 153–164.
Genetic variability of the threatened crayfish Austropotamobius italicus in Tuscany (Italy): implications for its management.Crossref | GoogleScholarGoogle Scholar |

Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., and Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |

Birky, C. W. (2013). Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS One 8, e52544.
Species detection and identification in sexual organisms using population genetic theory and DNA sequences.Crossref | GoogleScholarGoogle Scholar |

Buckup, L. (2010). Parastacus brasiliensis. The IUCN Red List of Threatened Species 2010, .
Parastacus brasiliensis.Crossref | GoogleScholarGoogle Scholar |

Buckup, L., and Bond-Buckup, G. (1994). Parastacidae e Aeglidae (Crustacea, Decapoda) Neotropicais do Museu de Berlim, Alemanha. Nauplius 2, 17–27.

Buckup, L., and Fontoura, N. F. (1989). Dinâmica populacional e reprodução em Parastacus brasiliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Revista Brasileira de Biologia 49, 911–921.

Buckup, L., and Rossi, A. (1980). O gênero Parastacus no Brasil (Crustacea, Decapoda, Parastacidae). Revista Brasileira de Biologia 40, 663–681.

Burnham, Q., and Dawkins, K. L. (2013). The role of molecular taxonomy in uncovering variation within crayfish and the implications for conservation. Freshwater Crayfish 19, 29–37.
The role of molecular taxonomy in uncovering variation within crayfish and the implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |

Cataudella, R., Paolucci, M., Delaunay, C., Ropiquet, A., Hassanin, A., Balsamo, M., and Grandjean, F. (2010). Genetic variability of Austropotamobius italicus in the Marches region: implications for conservation. Aquatic Conservation 20, 261–268.
Genetic variability of Austropotamobius italicus in the Marches region: implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Choleva, L., Musilova, Z., Kohoutova-Sediva, A., Paces, J., Rab, P., and Janko, K. (2014). Distinguishing between incomplete lineage sorting and genomic introgressions: complete fixation of allospecific mitochondrial DNA in a sexually reproducing fish (Cobitis; Teleostei), despite clonal reproduction of hybrids. PLoS One 9, e80641.
Distinguishing between incomplete lineage sorting and genomic introgressions: complete fixation of allospecific mitochondrial DNA in a sexually reproducing fish (Cobitis; Teleostei), despite clonal reproduction of hybrids.Crossref | GoogleScholarGoogle Scholar |

Clement, M., Posada, D., and Crandall, K. A. (2000). TCS : a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS : a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar |

Crandall, K. A., and De Grave, S. (2017). An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology 37, 615–653.
An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list.Crossref | GoogleScholarGoogle Scholar |

Crandall, K. A., and Fitzpatrick, J. F. (1996). Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Systematic Biology 45, 1–26.
Crayfish molecular systematics: using a combination of procedures to estimate phylogeny.Crossref | GoogleScholarGoogle Scholar |

Cumberlidge, N., Ng, P. K. L., Yeo, D. C. J., Magalhães, C., Campos, M. R., Alvarez, F., Naruse, T., Daniels, S. R., Esser, L. J., Attipoe, F. Y. K., Clotilde-Ba, F. L., Darwall, W., McIvor, A., Baillie, J. E. M., Collen, B., and Ram, M. (2009). Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges. Biological Conservation 142, 1665–1673.
Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges.Crossref | GoogleScholarGoogle Scholar |

Darwall, W. R., Holland, R. A., Smith, K. G., Allen, D., Brooks, E. G., Katarya, V., Pollock, C. M., Shi, Y., Clausnitzer, V., Cumberlidge, N., Cuttelod, A., Dijkstra, K. D. B., Diop, M. D., García, N., Seddon, M. B., Skelton, P. H., Snoeks, J., Tweddle, D., and Vié, J. C. (2011). Implications of bias in conservation research and investment for freshwater species. Conservation Letters 4, 474–482.
Implications of bias in conservation research and investment for freshwater species.Crossref | GoogleScholarGoogle Scholar |

Dawkins, K. L., Furse, J. M., Wild, C. H., and Hughes, J. M. (2010). Distribution and population genetics of the threatened freshwater crayfish genus Tenuibranchiurus (Decapoda: Parastacidae). Marine and Freshwater Research 61, 1048–1055.
Distribution and population genetics of the threatened freshwater crayfish genus Tenuibranchiurus (Decapoda: Parastacidae).Crossref | GoogleScholarGoogle Scholar |

Dawkins, K. L., Furse, J. M., Wild, C. H., and Hughes, J. M. (2017). A novel genus and cryptic species harboured within the monotypic freshwater crayfish genus Tenuibranchiurus Riek, 1951 (Decapoda: Parastacidae). PeerJ 5, e3310.
A novel genus and cryptic species harboured within the monotypic freshwater crayfish genus Tenuibranchiurus Riek, 1951 (Decapoda: Parastacidae).Crossref | GoogleScholarGoogle Scholar |

Diéguez-Uribeondo, J., Royo, F., Souty-Grosset, C., Ropiquet, A., and Grandjean, F. (2008). Low genetic variability of the white-clawed crayfish in the Iberian Peninsula: its origin and management implications. Aquatic Conservation: Marine and Freshwater Ecosystems 18, 19–31.
Low genetic variability of the white-clawed crayfish in the Iberian Peninsula: its origin and management implications.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar |

Ehrlich, P. R., and Wilson, E. O. (1991). Biodiversity studies: science and policy. Science 253, 758–762.
Biodiversity studies: science and policy.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., and Lischer, H. E. L. (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.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.Crossref | GoogleScholarGoogle Scholar |

Faxon, W. (1914). Notes on the crayfishes in the United States National Museum and the Museum of Comparative Zoölogy: with descriptions of new species and subspecies, to which is appended a catalogue of the known species and subspecie. Memoirs of the Museum of Comparative Zoölogy at Harvard College 40, 351–427.

Filipová, L., Holdich, D. M., Lesobre, J., Grandjean, F., and 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. Biological Invasions 12, 983–989.
Cryptic diversity within the invasive virile crayfish Orconectes virilis (Hagen, 1870) species complex: new lineages recorded in both native and introduced ranges.Crossref | GoogleScholarGoogle Scholar |

Fontoura, N. F., and Buckup, L. (1989). O crescimento de Parastacus brasiliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Revista Brasileira de Biologia 49, 897–909.

Fontoura, N. F., and Conter, M. R. (2008). Description of a new subspecies of the crayfish Parastacus brasiliensis (Von Martens, 1869) from São Francisco de Paula, RS, Brazil (Decapoda, Parastacidae). Zootaxa 1849, 28–34.

Fratini, S., Zaccara, S., Barbaresi, S., Grandjean, F., Souty-Grosset, C., Crosa, G., and Gherardi, F. (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 |

Fundação Estadual de Proteção Ambiental Henrique Luiz Roessler (FEPAM) (2010). Região Hidrográfica do Guaíba. Qualidade Ambiental. Available at: http://www.fepam.rs.gov.br/qualidade/guaiba.asp [accessed 2 January 2016].

Funk, D. J., and Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics 34, 397–423.
Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |

Gouin, N., Grandjean, F., and Souty-Grosset, C. (2006). Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications. Freshwater Biology 51, 1369–1387.
Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications.Crossref | GoogleScholarGoogle Scholar |

Grandjean, F., and Souty-Grosset, C. (2000). Genetic and morphological variation in the endangered crayfish species, Austropotamobius pallipes (Lereboullet) (Crustacea, Astacidae) from the Poitou-Charentes region (France). Aquatic Sciences 62, 1–19.
Genetic and morphological variation in the endangered crayfish species, Austropotamobius pallipes (Lereboullet) (Crustacea, Astacidae) from the Poitou-Charentes region (France).Crossref | GoogleScholarGoogle Scholar |

Gross, R., Palm, S., Kõiv, K., Prestegaard, T., Jussila, J., Paaver, T., Geist, J., Kokko, H., Karjalainen, A., and Edsman, L. (2013). Microsatellite markers reveal clear geographic structuring among threatened noble crayfish (Astacus astacus) populations in northern and central Europe. Conservation Genetics 14, 809–821.
Microsatellite markers reveal clear geographic structuring among threatened noble crayfish (Astacus astacus) populations in northern and central Europe.Crossref | GoogleScholarGoogle Scholar |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98. citeulike-article_id:691774

Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., and Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology 2, e312.
Identification of birds through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Helms, B. S., Suciu, S. K., Vaught, R. C., and Santos, S. R. (2015). Cryptic diversity within two endemic crayfish species of the southeastern US revealed by molecular genetics and geometric morphometrics. Hydrobiologia 755, 283–298.
Cryptic diversity within two endemic crayfish species of the southeastern US revealed by molecular genetics and geometric morphometrics.Crossref | GoogleScholarGoogle Scholar |

Hobbs, H. H. (1989). An illustrated checklist of the American crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae). Smithsonian Contributions to Zoology 480, 1–236.
An illustrated checklist of the American crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae).Crossref | GoogleScholarGoogle Scholar |

Huber, A. F., Ribeiro, F. B., and Araujo, P. B. (2018). New endemic species of freshwater crayfish Parastacus Huxley, 1879 (Crustacea: Decapoda: Parastacidae) from the Atlantic forest in southern Brazil. Nauplius 26, e2018015.
New endemic species of freshwater crayfish Parastacus Huxley, 1879 (Crustacea: Decapoda: Parastacidae) from the Atlantic forest in southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Humphries, C. J., Williams, P. H., and Wright, R. I. V. (1995). Measuring biodiversity value for conservation. Annual Review of Ecology and Systematics 26, 93–111.
Measuring biodiversity value for conservation.Crossref | GoogleScholarGoogle Scholar |

Huxley, T. H. (1879). On the classification and the distribution of the crayfishes. Proceedings of the Zoological Society of London 1878, 752–788.
On the classification and the distribution of the crayfishes.Crossref | GoogleScholarGoogle Scholar |

IUCN (2016). The IUCN Red List of Threatened Species. Available at: https://www.iucnredlist.org/technical-documents/categories-and-criteria

Jesse, R., Schubart, C. D., and Klaus, S. (2010). Identification of a cryptic lineage within Potamon fluviatile (Herbst) (Crustacea: Brachyura: Potamidae). Invertebrate Systematics 24, 348–356.
Identification of a cryptic lineage within Potamon fluviatile (Herbst) (Crustacea: Brachyura: Potamidae).Crossref | GoogleScholarGoogle Scholar |

Kawai, T., and Crandall, K. A. (2016). Global diversity and conservation of freshwater crayfish (Crustacea: Decapoda: Astacoidea). In ‘A Global Overview of the Conservation of Freshwater Decapod Crustaceans’. (Eds T. Kawai and N. Cumberlidge.) pp. 64–114. (Springer: Cham.) 10.1007/978-3-319-42527-6_3

Koizumi, I., Usio, N., Kawai, T., Azuma, N., and Masuda, R. (2012). Loss of genetic diversity means loss of geological information: the endangered Japanese crayfish exhibits remarkable historical footprints. PLoS One 7, e33986.
Loss of genetic diversity means loss of geological information: the endangered Japanese crayfish exhibits remarkable historical footprints.Crossref | GoogleScholarGoogle Scholar |

Langone, J. A., Camargo, A., and de Sá, R. O. (2016). High genetic diversity but low population structure in the frog Pseudopaludicola falcipes (Hensel, 1867) (Amphibia, Anura) from the Pampas of South America. Molecular Phylogenetics and Evolution 95, 137–151.
High genetic diversity but low population structure in the frog Pseudopaludicola falcipes (Hensel, 1867) (Amphibia, Anura) from the Pampas of South America.Crossref | GoogleScholarGoogle Scholar |

Larson, E. R., Abbott, C. L., Usio, N., Azuma, N., Wood, K. A., Herborg, L. M., and Olden, J. D. (2012). The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific Northwest range of Pacifastacus leniusculus. Freshwater Biology 57, 1823–1838.
The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific Northwest range of Pacifastacus leniusculus.Crossref | GoogleScholarGoogle Scholar |

Larson, E. R., Castelin, M., Williams, B. W., Olden, J. D., and Abbott, C. L. (2016). Phylogenetic species delimitation for crayfishes of the genus Pacifastacus. PeerJ 4, .
Phylogenetic species delimitation for crayfishes of the genus Pacifastacus.Crossref | GoogleScholarGoogle Scholar |

Lewis, O. T., and Senior, M. J. M. (2011). Assessing conservation status and trends for the world’s butterflies: the sampled Red List Index approach. Journal of Insect Conservation 15, 121–128.
Assessing conservation status and trends for the world’s butterflies: the sampled Red List Index approach.Crossref | GoogleScholarGoogle Scholar |

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

Magris, R. M., Bond-Buckup, G., Magalhães, C., Mantelatto, F. L., Reid, J. W., Loureiro, L. M. E., Coelho, P. A., Santana, W., Buckup, L., Rocha, S. S., Bueno, S. L. S., Pinheiro, M. A. A., D’Incao, F., Ivo, C. T. C., Neto, J. D., Rodrigues, E. S., Araújo, P. B., Boos, H., and Duarte, L. F. A. (2010). Quantification of extinction risk for crustacean species: an overview of the National Red Listing process in Brazil. Nauplius 18, 129–135.

Maguire, I., Podnar, M., Jelić, M., Štambuk, A., Schrimpf, A., Schulz, H., and Klobučar, G. (2014). Two distinct evolutionary lineages of the Astacus leptodactylus species-complex (Decapoda: Astacidae) inferred by phylogenetic analyses. Invertebrate Systematics 28, 117–123.
Two distinct evolutionary lineages of the Astacus leptodactylus species-complex (Decapoda: Astacidae) inferred by phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |

Martens, E. von (1869). Südbrasilianische Süss-und Brackwasser-Crustaceen nach den Sammlungen des Dr. Reinh. Hensel. Archiv für Naturgeschichte 35, 1–37.

Mathews, L. M., Adams, L., Anderson, E., Basile, M., Gottardi, E., and Buckholt, M. A. (2008). Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex. Molecular Phylogenetics and Evolution 48, 126–135.
Genetic and morphological evidence for substantial hidden biodiversity in a freshwater crayfish species complex.Crossref | GoogleScholarGoogle Scholar |

Miller, M. P. (2005). Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. The Journal of Heredity 96, 722–724.
Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information.Crossref | GoogleScholarGoogle Scholar |

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘2010 Gateway Computing Environments Workshop (GCE)’. pp. 1–8. Available at: 10.1109/GCE.2010.5676129

Moraes, J. C. B., Terossi, M., Buranelli, R. C., Tavares, M., Mantelatto, F. L., Luiz, S., and Bueno, S. L. S. (2016). Morphological and molecular data reveal the cryptic diversity among populations of Aegla paulensis (Decapoda, Anomura, Aeglidae), with descriptions of four new species and comments on dispersal routes and conservation status. Zootaxa 4193, 1–48.
Morphological and molecular data reveal the cryptic diversity among populations of Aegla paulensis (Decapoda, Anomura, Aeglidae), with descriptions of four new species and comments on dispersal routes and conservation status.Crossref | GoogleScholarGoogle Scholar |

Ortmann, A. E. (1902). The geographical distribution of freshwater decapods and its bearing upon ancient geography. Proceedings of the American Philosophical Society 41, 267–400.

Palaoro, A. V., del Valle, E., and Thiel, M. (2016). Life history patterns are correlated with predictable fluctuations in highly seasonal environments of semi-terrestrial burrowing crayfish. Hydrobiologia 767, 51–63.
Life history patterns are correlated with predictable fluctuations in highly seasonal environments of semi-terrestrial burrowing crayfish.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A. (2017). FigTree 1.4.3. Available at: http://tree.bio.ed.ac.uk/sofware/fgtree/

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer

Ribeiro, F. B., and Araujo, P. B. (2017). Designation of a neotype for Parastacus nicoleti (Philippi, 1882) (Crustacea: Decapoda: Parastacidae). Zootaxa 4338, 393–400.
Designation of a neotype for Parastacus nicoleti (Philippi, 1882) (Crustacea: Decapoda: Parastacidae).Crossref | GoogleScholarGoogle Scholar |

Ribeiro, F. B., Buckup, L., Gomes, K. M., and Araujo, P. B. (2016). Two new species of South American freshwater crayfish genus Parastacus Huxley, 1879 (Crustacea: Decapoda: Parastacidae). Zootaxa 4158, 301–324.
Two new species of South American freshwater crayfish genus Parastacus Huxley, 1879 (Crustacea: Decapoda: Parastacidae).Crossref | GoogleScholarGoogle Scholar |

Ribeiro, F. B., Huber, A. F., Schubart, C. D., and Araujo, P. B. (2017). A new species of Parastacus Huxley, 1879 (Crustacea, Decapoda, Parastacidae) from a swamp forest in southern Brazil. Nauplius 25, e2017008.
A new species of Parastacus Huxley, 1879 (Crustacea, Decapoda, Parastacidae) from a swamp forest in southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Richman, N. I., Bohm, M., Adams, S. B., Alvarez, F., Bergey, E. A., Bunn, J. J. S., Burnham, Q., Cordeiro, J., Coughran, J., Crandall, K. A., Dawkins, K. L., DiStefano, J., Doran, N. E., Edsman, L., Eversole, A. G., Füreder, L., Furse, J. M., Gherardi, F., Hamr, P., Holdich, D. M., Horwitz, P., Johnston, K., Jones, C. M., Jones, J. P. G., Jones, R. L., Jones, T. G., Kawai, T., Lawler, S., Lópex-Mejía, M., Miller, R. M., Pedraza-Lara, C., Reynolds, J. D., Richardson, A. M. M., Schultz, M. B., Schuster, G. A., Sibley, P. J., Souty-Grosset, C., Taylor, A., Thoma, R. F., Walls, J., Walsh, T. S., and Collen, B. (2015). Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea). Philosophical Transaction of the Royal Society B 370, 20140060.
Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea).Crossref | GoogleScholarGoogle Scholar |

Riek, E. F. (1971). The freshwater crayfishes of South America. Proceedings of the Biological Society of Washington 84, 129–136.
The freshwater crayfishes of South America.Crossref | GoogleScholarGoogle Scholar |

Rogers, A. R., and Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
Population growth makes waves in the distribution of pairwise genetic differences.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3. 2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3. 2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |

Rudolph, E. H. (2013). A checklist of the Chilean Parastacidae (Decapoda, Astacidea). Crustaceana 86, 1468–1510.
A checklist of the Chilean Parastacidae (Decapoda, Astacidea).Crossref | GoogleScholarGoogle Scholar |

Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M. A., and Barrell, B. (2000). Artemis: sequence visualization and annotation. Bioinformatics 16, 944–945.
Artemis: sequence visualization and annotation.Crossref | GoogleScholarGoogle Scholar |

Schneider, S., and Excoffier, L. (1999). Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152, 1079–1089.

Schubart, C. D. (2009). Mitochondrial DNA and decapod phylogenies; the importance of pseudogenes and primer optimization. In ‘Crustacean Issues: Decapod Crustacean Phylogenetics’. (Eds J. W. Martin, K. A. Crandall, and D. L. Felder.) pp. 47–65. (CRC Press: Boca Raton, FL.)

Schubart, C. D., Cuesta, J. A., and Felder, D. L. (2002). Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea. Journal of Crustacean Biology 22, 28–44.
Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea.Crossref | GoogleScholarGoogle Scholar |

Schultz, M. B., Smith, S. A., Richardson, A. M. M., Horwitz, P., Crandall, K. A., and Austin, C. M. (2007). Cryptic diversity in Engaeus Erichson, Geocharax Clark and Gramastacus Riek (Decapoda : Parastacidae) revealed by mitochondrial 16S rDNA sequences. Invertebrate Systematics 21, 569–587.
Cryptic diversity in Engaeus Erichson, Geocharax Clark and Gramastacus Riek (Decapoda : Parastacidae) revealed by mitochondrial 16S rDNA sequences.Crossref | GoogleScholarGoogle Scholar |

Schwarz, G. (1978). Estimating the dimension of a model. The Annals of Statistics 6, 461–464.
Estimating the dimension of a model.Crossref | GoogleScholarGoogle Scholar |

SEMA – Secretaria do Ambiente e Desenvolvimento Sustentável. (2018). Base Cartográfica do Estado do Rio Grande do Sul, escala 1:25.000 – BCRS25 – versão 1.0. Available at http://sema.rs.gov.br/cartografia

Sinclair, E. A., Madsen, A., Walsh, T., Nelson, J., and Crandall, K. A. (2011). Cryptic genetic divergence in the giant Tasmanian freshwater crayfish Astacopsis gouldi (Decapoda: Parastacidae): implications for conservation. Animal Conservation 14, 87–97.
Cryptic genetic divergence in the giant Tasmanian freshwater crayfish Astacopsis gouldi (Decapoda: Parastacidae): implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Slatkin, M., and Hudson, R. R. (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.

Song, H., Buhay, J. E., Whiting, M. F., and Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105, 13486–13491.
Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified.Crossref | GoogleScholarGoogle Scholar |

Souty-Grosset, C., and Fetzner, J. W. (2016). Taxonomy and identification. In ‘Biology and Ecology of Crayfish’. (Eds M. Longshaw, and P. Stebbing.) pp. 1–30. (CRC Press.) 10.1201/b20073-2

Souza-Carvalho, E. A., Magalhães, C., and Mantelatto, F. L. (2017). Molecular phylogeny of the Trichodactylus fluviatilis species complex. Journal of Crustacean Biology 37, 187–194.
Molecular phylogeny of the Trichodactylus fluviatilis species complex.Crossref | GoogleScholarGoogle Scholar |

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar |

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.Crossref | GoogleScholarGoogle Scholar |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Crossref | GoogleScholarGoogle Scholar |

Thiercelin, N., and Schubart, C. D. (2014). Transisthmian differentiation in the tree-climbing mangrove crab Aratus H. Milne Edwards, 1853 (Crustacea, Brachyura, Sesarmidae), with description of a new species from the tropical eastern Pacific. Zootaxa 3793, 545–560.
Transisthmian differentiation in the tree-climbing mangrove crab Aratus H. Milne Edwards, 1853 (Crustacea, Brachyura, Sesarmidae), with description of a new species from the tropical eastern Pacific.Crossref | GoogleScholarGoogle Scholar |

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 |

Toon, A., Pérez-Losada, M., Schweitzer, C. E., Feldmann, R. M., Carlson, M., and Crandall, K. A. (2010). Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules. Journal of Biogeography 37, 2275–2290.
Gondwanan radiation of the Southern Hemisphere crayfishes (Decapoda: Parastacidae): evidence from fossils and molecules.Crossref | GoogleScholarGoogle Scholar |

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 |

Xia, X. (2013). DAMBE5 : a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 1720–1728.
DAMBE5 : a comprehensive software package for data analysis in molecular biology and evolution.Crossref | GoogleScholarGoogle Scholar |

Xia, X., Xie, Z., Salemi, M., Chen, L., and Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.
An index of substitution saturation and its application.Crossref | GoogleScholarGoogle Scholar |

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 |

Zhou, Y., Duvaux, L., Ren, G., Zhang, L., Savolainen, O., and Liu, J. (2016). Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions. Heredity 118, 211–220.
Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions.Crossref | GoogleScholarGoogle Scholar |