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

Porcelain crabs of the genera Pachycheles Stimpson and Neopisosoma Haig (Decapoda : Anomura : Porcellanidae): new premises based on molecular data and comments on phylogenetic relationships in the family

Ivana Miranda A and Fernando L. Mantelatto B C
+ Author Affiliations
- Author Affiliations

A Biologie I, Universität Regensburg, 93040, Regensburg, Germany.

B Laboratory of Bioecology and Crustacean Systematics (LBSC), Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Av. Bandeirantes 3900, CEP 14040-901, Ribeirão Preto, São Paulo, Brazil.

C Corresponding author. Email: flmantel@usp.br

Invertebrate Systematics 30(5) 509-520 https://doi.org/10.1071/IS16025
Submitted: 22 November 2015  Accepted: 20 May 2016   Published: 31 October 2016

Abstract

Porcellanidae Haworth, 1825 is a family of marine anomuran crabs distributed throughout tropical and temperate regions of all the oceans, typically littoral and sublittoral waters, with a considerable diversity of lifestyles, habitats and colouration. Pachycheles Stimpson, 1858 and Neopisosoma Haig, 1960 share, among other morphological characteristics, the fragmentation of the lateral carapace walls. The morphology of this body region was key to supporting the establishment of Neopisosoma, which increased uncertainty about the taxonomic status of these genera due to the high intraspecific variation of this character. Our study reconstructs the phylogenetic relationship between Pachycheles and Neopisosoma based on mitochondrial and nuclear DNA sequences to evaluate whether these are valid taxa. While Pachycheles seems to be monophyletic, the position of Neopisosoma mexicanum (Streets, 1871) indicates that the group is polyphyletic, and deserves further investigation. Pachycheles is revealed to be older than Neopisosoma, and likely originated in the Indo-Pacific, later spreading to the American continent during the early Tertiary. Neopisosoma may have arisen much later in the Caribbean Province before the closure of the Isthmus of Panama, explaining its distribution, which is restricted mainly to Central America. The inclusion of a considerable number of species from both genera represents a significant advance in the study of this controversial group. The phylogenetic reconstruction of Pachycheles unveiled clades corroborated by morphology, but also revealed unclear relationships, which may indicate the potential existence of cryptic species.

Additional keywords: Crustacea, mitochondrial DNA, molecular taxonomic, nuclear DNA.


References

Beschin, C., Busulini, A., De Angeli, A., and Tessier, G. (2007). ‘I decapodi dell’Eocene inferiore di Contrada Gecchelina (Vicenza – Italia settentrionale) (Anomura e Brachiura).’ (Museo di Archeologia e Scienze Naturali ‘G. Zannato’: Montecchio Maggiore, Vicenza.)

Boschi, E. E. (1963). Sobre dos especies de Pachycheles de la Argentina (Crustacea, Anomura). Neotrópica 9, 31–37.

Bracken-Grissom, H. D., Cannon, M. E., Cabezas, P., Feldmann, R. M., Schweitzer, C. E., Ahyong, S. T., Felder, D. L., Lemaitre, R., and Crandall, K. A. (2013). A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda). BMC Evolutionary Biology 13, 128.
A comprehensive and integrative reconstruction of evolutionary history for Anomura (Crustacea: Decapoda).Crossref | GoogleScholarGoogle Scholar | 23786343PubMed |

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 | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=7270e7b94b46ec4a30ad5328609b8552CAS | 10742046PubMed |

Colgan, D. J., McLauchlan, A., Wilson, G. D. F., Livingston, S. P., Edgecombe, G. D., Macaranas, J., Cassis, G., and Gray, M. R. (1998). Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology 46, 419–437.
Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution.Crossref | GoogleScholarGoogle Scholar |

Crandall, K., Harris, D. J., and Fetzner, J. W. (2000). The monophyletic origin of freshwater crayfish estimated from nuclear and mitochondrial DNA sequences. Proceedings. Biological Sciences 267, 1679–1686.
The monophyletic origin of freshwater crayfish estimated from nuclear and mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFSiu7c%3D&md5=3d4fef85d908a5b9ab5906e6050f43e7CAS | 11467432PubMed |

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 | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=5ab730c939a1ffbe2d25920cbdfa4ea5CAS | 22367748PubMed |

Gore, R. H. (1977). Neopisosoma angustifrons (Benedict, 1901): the complete larval development under laboratory conditions, with notes on larvae of the related genus Pachycheles (Decapoda Anomura, Porcellanidae). Crustaceana 33, 284–300.
Neopisosoma angustifrons (Benedict, 1901): the complete larval development under laboratory conditions, with notes on larvae of the related genus Pachycheles (Decapoda Anomura, Porcellanidae).Crossref | GoogleScholarGoogle Scholar |

Gore, R. H., and Abele, L. G. (1973). Three new species of porcellanid crabs (Crustacea, Decapoda, Porcellanidae) from the Bay of Panama and adjacent Caribbean waters. Bulletin of Marine Science 23, 559–573.

Grant, T., and Kluge, A. G. (2003). Data exploration in phylogenetic inference: scientific, heuristic, or neither. Cladistics 19, 379–418.
Data exploration in phylogenetic inference: scientific, heuristic, or neither.Crossref | GoogleScholarGoogle Scholar |

Haig, J. (1956). The Galatheidae (Crustacea Anomura) of the Allan Hancock Expedition with a review of the Porcellanidae of the Western North Atlantic. Allan Hancock Atlantic Expedition, 1–44.

Haig, J. (1960). The Porcellanidae (Crustacea Anomura) of the Eastern Pacific. Allan Hancock Foundation Pacific Expeditions, 1–440.

Hiller, A., Kraus, H., Almon, M., and Werding, B. (2006). The Petrolisthes galathinus complex: species boundaries based on color pattern, morphology and molecules, and evolutionary interrelationships between this complex and other Porcellanidae (Crustacea: Decapoda: Anomura). Molecular Phylogenetics and Evolution 40, 547–569.
The Petrolisthes galathinus complex: species boundaries based on color pattern, morphology and molecules, and evolutionary interrelationships between this complex and other Porcellanidae (Crustacea: Decapoda: Anomura).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntFWqsbw%3D&md5=e32b17e412f0858be9a731b0ce261658CAS | 16684610PubMed |

Hultgren, K. M., and Stachowicz, J. J. (2008). Molecular phylogeny of the brachyuran crab superfamily Majoidea indicates close congruence with trees based on larval morphology. Molecular Phylogenetics and Evolution 48, 986–996.
Molecular phylogeny of the brachyuran crab superfamily Majoidea indicates close congruence with trees based on larval morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyntLrF&md5=4a60f6f9592684cf272df3c8c1f9deadCAS | 18621552PubMed |

Konishi, K. (1987). The larval development of Pachycheles stevensii Stimpson, 1858 (Crustacea: Anomura: Porcellanidae) under laboratory conditions. Journal of Crustacean Biology 7, 481–492.
The larval development of Pachycheles stevensii Stimpson, 1858 (Crustacea: Anomura: Porcellanidae) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |

Mantelatto, F. L., Robles, R., Biagi, R., and Felder, D. L. (2006). Molecular analysis of the taxonomic and distributional status for the hermit crab genera Loxopagurus Forest, 1964 and Isocheles Stimpson, 1858 (Decapoda, Anomura, Diogenidae). Zoosystema 1858, 495–506.

Mantelatto, F. L., Robles, R., and Felder, D. L. (2007). Molecular phylogeny of the western Atlantic species of the genus Portunus (Crustacea, Brachyura, Portunidae). Zoological Journal of the Linnean Society 150, 211–220.
Molecular phylogeny of the western Atlantic species of the genus Portunus (Crustacea, Brachyura, Portunidae).Crossref | GoogleScholarGoogle Scholar |

Mantelatto, F. L., Pardo, L. M., Pileggi, L. G., and Felder, D. L. (2009a). Taxonomic re-examination of the hermit crab species Pagurus forceps and Pagurus comptus (Decapoda: Paguridae) by molecular analysis. Zootaxa 32, 20–32.

Mantelatto, F. L., Robles, R., Schubart, C. D., and Felder, D. L. (2009b). Molecular phylogeny of the genus Cronius Stimpson, 1860, with reassignment of C. tumidulus and several American species of Portunus to the genus Achelous De Haan, 1833 (Brachyura: Portunidae). In ‘Decapod Crustacean Phylogenetics’. pp. 551–565. 10.1201/9781420092592-c29

Mantelatto, F. L., Pileggi, L. G., Miranda, I., and Wehrtmann, I. S. (2011). Does Petrolisthes armatus (Anomura, Porcellanidae) form a species complex or are we dealing with just one widely distributed species? Zoological Studies 50, 372–384.

Melo, G. A. S. (1999). ‘Manual de Identificação dos Crustacea Decapoda do Litoral Brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea.’ (Ed. Plêidae: São Paulo, Brazil.)

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE), 1–8. 10.1109/GCE.2010.5676129

Miranda, I., Schubart, C. D., and Mantelatto, F. L. (2014). Morphological and molecular data support the distinctiveness of Pachycheles laevidactylus Ortmann, 1892 and Pachycheles chubutensis Boschi, 1963. Zootaxa 3852, 118–132.
Morphological and molecular data support the distinctiveness of Pachycheles laevidactylus Ortmann, 1892 and Pachycheles chubutensis Boschi, 1963.Crossref | GoogleScholarGoogle Scholar |

Ortmann, A. E. (1897). Carcinologische studien. Zoologische Jahrbucher 10, 258–372.

Osawa, M., and Mclaughlin, P. A. (2010). Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea). Part II – Porcellanidae. The Raffles Bulletin of Zoology 23, 109–129.

Patwardhan, A., Ray, S., and Roy, A. (2014). Molecular markers in phylogenetic studies – a review. Journal of Phylogenetics & Evolutionary Biology 2, 1–9.

Pileggi, L. G., and Mantelatto, F. L. (2010). Molecular phylogeny of the freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae), with emphasis on the relationships among selected American species. Invertebrate Systematics 24, 194–208.
Molecular phylogeny of the freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae), with emphasis on the relationships among selected American species.Crossref | GoogleScholarGoogle Scholar |

Por, D. F. (1989). ‘The Legacy of Tethys.’ 10.1007/978-94-009-0937-3

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer (Acessed at October/2015)

Rodríguez, I. T., Hernandez, G., Magán, I., Bolaños, J., and Felder, D. L. (2004). Larval development of Pachycheles serratus (Decapoda: Anomura: Porcellanidae) under laboratory conditions, with notes on the larvae of the genus. Journal of Crustacean Biology 24, 291–308.
Larval development of Pachycheles serratus (Decapoda: Anomura: Porcellanidae) under laboratory conditions, with notes on the larvae of the genus.Crossref | GoogleScholarGoogle Scholar |

Rodríguez, I. T., Hernández, G., and Felder, D. L. (2005). Review of the western Atlantic Porcellanidae (Crustacea: Decapoda: Anomura) with new records, systematic observations, and comments on biogeography. Caribbean Journal of Science 41, 544–582.

Rodríguez, I. T., Hernández, G., and Felder, D. L. (2006). Phylogenetic relationships among western Atlantic Porcellanidae (Decapoda: Anomura), based on partial sequences of the mitochondrial 16s rRNA gene, with comments on morphology. Crustacean Research, Special Number 6, 151–166.

Rossi, N., and Mantelatto, F. L. (2013). Molecular analysis of the freshwater prawn Macrobrachium olfersii (Decapoda, Palaemonidae) supports the existence of a single species throughout its distribution. PLoS One 8, e54698.
Molecular analysis of the freshwater prawn Macrobrachium olfersii (Decapoda, Palaemonidae) supports the existence of a single species throughout its distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1ymt74%3D&md5=485e20e5292a43542a2e8ea8079e27e9CAS | 23382941PubMed |

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 | 1:CAS:528:DC%2BD3MXjvVWksw%3D%3D&md5=762ad44096d50ed9ee640cd96effed87CAS | 11120685PubMed |

Schubart, C. D. (2009). Mitocondrial 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 Taylor and Francis Group: Boca Raton, FL.) 10.1080/17451001003604796

Schubart, C. D., Cuesta, J. A., Diesel, R., and Felder, D. L. (2000a). Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 15, 179–190.
Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs12qtbk%3D&md5=5d1033802659b058d950f367a0269c94CAS | 10837150PubMed |

Schubart, C. D., Neigel, J. E., and Felder, D. L. (2000b). Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. In ‘Crustacean Issues’. (Eds von V. Klein, J. Carel, and F. R. Schram.) pp. 817–830. (CRC Press Taylor and Francis Group: Boca Raton, FL.)

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 | 1:CAS:528:DC%2BD1cXhtFChs7vP&md5=963e2d5821d6c938bba7442562dd06d5CAS | 18757756PubMed |

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 | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=75f7f4dcbee031d89a4fac72e69aca2fCAS | 16928733PubMed |

Stillman, J. H., and Reeb, C. A. (2001). Molecular phylogeny of Eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications. Molecular Phylogenetics and Evolution 19, 236–245.
Molecular phylogeny of Eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1GmsLo%3D&md5=4ce38af395751cdedfbdc3423db43d8aCAS | 11341806PubMed |

Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=e6aee5793349cd5b40115c3d6e045e10CAS | 17654362PubMed |

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 | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=03ff7cc7d33ff928f46a243ed7d97fb2CAS | 24132122PubMed |

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=7172d8430c492515869dd831befd6b0eCAS | 7984417PubMed |

Timm, L., and Bracken-Grissom, H. (2015). The forest for the trees: evaluating molecular phylogenies with an emphasis on higher-level Decapoda Latreille, 1802. Journal of Crustacean Biology 35, 577–592.
The forest for the trees: evaluating molecular phylogenies with an emphasis on higher-level Decapoda Latreille, 1802.Crossref | GoogleScholarGoogle Scholar |

Vergamini, F. G., Pileggi, L. G., and Mantelatto, F. L. (2011). Genetic variability of the Amazon River prawn Macrobrachium amazonicum (Decapoda, Caridea, Palaemonidae). Contributions to Zoology (Amsterdam, Netherlands) 80, 67–83.

Werding, B. (1986). Die Gattung Neopisosoma Haig, 1960 im tropischen Westatlantic, mit der beschreibung von Neopisosoma neglectum spec. nov. und Neopisosoma orientale spec. nov. (Crustacea: Anomura: Porcellanidae). Rijksmuseum van Natuurlijke Historie te Leiden 60, 159–179.

Werding, B., and Müller, H.-G. (1990). Larval development of Neopisosoma neglectum Werding, 1986 (Decapoda: Anomura: Porcellanidae) under laboratory conditions. Helgolaender Meeresuntersuchungen 44, 363–374.
Larval development of Neopisosoma neglectum Werding, 1986 (Decapoda: Anomura: Porcellanidae) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |

Werding, B., Hiller, A., and Misof, B. (2001). Evidence of paraphyly in the neotropical Porcellanid genus Neopisosoma (Crustacea: Anomura: Porcellanidae) based on molecular characters. Hydrobiologia 449, 105–110.
Evidence of paraphyly in the neotropical Porcellanid genus Neopisosoma (Crustacea: Anomura: Porcellanidae) based on molecular characters.Crossref | GoogleScholarGoogle Scholar |

Werding, B., Hiller, A., and Lemaitre, R. (2003). Geographic and depth distributional patterns of western Atlantic Porcellanidae (Crustacea: Decapoda: Anomura), with an updated list of species. Memoirs of the Museum of Victoria 60, 79–85.

Wheeler, W. C. (1995). Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Systematic Biology 44, 321–331.
Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data.Crossref | GoogleScholarGoogle Scholar |

Wheeler, W. C. (1996). Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1–9.
Optimization alignment: the end of multiple sequence alignment in phylogenetics?Crossref | GoogleScholarGoogle Scholar |

Wheeler, W. C., Lucaroni, N., Hong, L., Crowley, L. M., and Varón, A. (2014). POY version 5: phylogenetic analysis using dynamic homologies under multiple optimality criteria. Cladistics 1997, 1–8.

Woodring, W. P. (1974). The Miocene Caribbean faunal province and its subprovinces. Verhandlungen der Naturforschenden Gesellschaft in Basel 84, 209–213.