Further polyphyly of pinnotheroid crabs: the molecular phylogenetic position of the polychaete-associated Aphanodactylidae
Ling Ming Tsang A , Shane T. Ahyong B E , Hsi-Te Shih C and Peter K. L. Ng DA Institute of Marine Biology, National Taiwan Ocean University, Keelung 202, Taiwan.
B Australian Museum Research Institute, 1 William St, Sydney, NSW 2010, Australia, and School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW 2052, Australia.
C Department of Life Science and Research Center for Global Change Biology, National Chung Hsing University, Taichung 402, Taiwan.
D Lee Kong Chian Natural History Museum, Faculty of Science, National University of Singapore, 2 Conservatory Drive, Singapore 117377, Singapore.
E Corresponding author. Email: Shane.Ahyong@austmus.gov.au
Invertebrate Systematics 32(1) 92-99 https://doi.org/10.1071/IS17038
Submitted: 11 April 2017 Accepted: 1 June 2017 Published: 9 January 2018
Abstract
Pea crabs of the superfamily Pinnotheroidea De Haan, 1833 are known for their obligate commensal relationships with other marine invertebrates. The concomitant specialisations and adaptations of pinnotheroids have resulted in superficially similar body forms that include a high degree of structural reduction. This has confounded interpretation of their phylogenetic position in the Brachyura and interrelationships within Pinnotheroidea, though all were nevertheless believed to be united by a monophyletic origin of obligate commensalism. The family Aphanodactylidae Ahyong & Ng, 2009 was proposed for a group of genera associated with tube-dwelling polychaetes formerly classified in Pinnotheridae, and provisionally retained in the Pinnotheroidea. We investigated the phylogenetic position of Aphanodactylidae using molecular data from three markers (mitochondrial 12S and 16S rRNAs, and nuclear histone H3) covering five of the 12 described aphanodactylid species and a total of 15 thoracotreme families. We found Aphanodactylidae to be monophyletic, but widely distant from Pinnotheridae and instead most closely related to Macrophthalmidae (Ocypodoidea) and Varunidae (Grapsoidea). Therefore, the family Aphanodactylidae is corroborated, but its placement in Pinnotheroidea is rejected. Instead, the phylogenetic position of Aphanodactylidae, as clearly distant from other pinnotheroids, demonstrates that obligate commensalism has evolved independently multiple times within Thoracotremata.
References
Ahyong, S. T., and Ng, P. K. L. (2009). Aphanodactylidae, a new family of thoracotreme crabs (Crustacea: Brachyura) symbiotic with polychaete worms. Zootaxa 2289, 33–47.Balss, H. (1934). Die Krabben der Reise J.W. Harms’ nach der Christmas-Insel und dem Malaiischen Archipel. Zoologischer Anzeiger 106, 225–237.
Benedict, J. E. (1892). Decapod Crustacea of Kingston Harbour. Johns Hopkins University Circular 11, 77.
Bürger, O. (1895). Ein beitrag zur kenntniss der pinnotherinen. Zoologische Jahrbucher. Abteilung fur Systematik, Geographie und Biologie der Tiere 8, 361–390.
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=1b4ae107a4d41c6cf044947b82a73459CAS |
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.
Crane, J. (1975). ‘Fiddler Crabs of the World (Ocypodidae: Genus Uca).’ (Princeton University Press: Princeton, NJ.)
Crosnier, A. (1965). Crustacés décapodes. Grapsidae et Ocypodidae. Faune de Madagascar 18, 1–143.
Dai, A.-Y., Song, Y.-Z., and Yang, S.-L. (1985). A study on Ocypode from China (Crustacea: Decapoda). Dong Wu Fen Lei Xue Bao 10, 370–378.
Dana, J. D. (1851). Conspectus Crustaceorum quae in Orbis Terrarum circumnavigatione, Carolo Wilkes e Classe Reipublicae Foederatae Duce, lexit et descripsit J.D. Dana. – Pars VI. American Journal of Science and Arts, Series 2 11, 268–274.
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=8455a3ff18c54ee00d48a1421d4dba7aCAS |
Davie, P. J. F., Guinot, D., and Ng, P. K. L. (2016). Systematics and classification of Brachyura. In ‘Treatise of Zoology – Anatomy, Taxonomy, Biology. The Crustacea. Volume 9. Part C–II Decapod: Brachyura’. (Eds P. Castro, P. J. F. Davie, D. Guinot, F. R. Schram and J. C. von Vaupel Klein.) pp. 1049–1130. (Brill: Leiden, Netherlands.)
De Man, J. G. (1892). Decapoden des Indischen Archipels. In ‘Zoologische Ergebnisse einer Reise in Niederländisch Ost-Indien. Vol. 2’. (Ed. M. Weber.) pp. 265–527, pls 15–29. (Leyden Museum: Leyden.)
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=9f0ae72ae0dad8d77ae7a57341dd73f7CAS |
Glassell, S. A. (1933). Description of five new species of Brachyura collected on the west coast of Mexico. Transactions of the San Diego Society of Natural History 7, 331–334.
Herbst, J. F. W. (1790). ‘Versuch einer Naturgeschichte der Krabben und Krebse nebst einer systematischen Beschreibung ihrer verschieden Arten. Vol. 1, Part 8’. pp. 239–274, pls 18–21. (Gottlieb August Lange: Berlin.)
Herbst, J. F. W. (1804). ‘Versuch einer Naturgeschichte der Krabben und Krebse nebst einer systematischen Beschreibung ihrer verschieden Arten. Vol. 3, Part 4’. pp. 1–49, pls 59–62. (Gottlieb August Lange: Berlin.)
Kemp, S. (1919). Notes on Crustacea Decapoda in the Indian Museum. XII. Scopimerinae. Records of the Indian Museum 16, 305–348.
Kitaura, J., Wada, K., and Nishida, M. (2002). Molecular phylogeny of grapsoid and ocypodoid crabs with special reference to the genera Metaplax and Macrophthalmus. Journal of Crustacean Biology 22, 682–693.
| Molecular phylogeny of grapsoid and ocypodoid crabs with special reference to the genera Metaplax and Macrophthalmus.Crossref | GoogleScholarGoogle Scholar |
Komai, T. (2011). A new species of the varunid crab genus Gopkittisak (Crustacea: Decapoda: Bracyhura: Grapsoidea) from the Ryukyu Islands. Species Diversity 16, 103–111.
Komai, T., and Konishi, K. (2012). Reappraisal of the systematic position of the supposed pinnotherid crab Pseudopinnixa carinata (Crustacea: Decapoda: Brachyura). Species Diversity 17, 29–37.
| Reappraisal of the systematic position of the supposed pinnotherid crab Pseudopinnixa carinata (Crustacea: Decapoda: Brachyura).Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=bcbd369c661cdc481de05ecb4f74d120CAS |
Linnaeus, C. (1767). ‘Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis.’ 12th edn. Vol. 1. Vindoboniae. pp. 533–1327. (Laurentii Salvii: Holmiae.)
MacLeay, W. S. (1838). On the brachyurous decapod Crustacea brought from the Cape by Dr Smith. In ‘Illustrations of the Zoology of South Africa; Consisting Chiefly of Figures and Descriptions of the Objects of Natural History Collected During an Expedition into the Interior of South Africa, in the Years 1834, 1835, and 1836; Fitted out by ‘The Cape of Good Hope Association for Exploring Central Africa’: Together with a Summary of African Zoology, and an Inquiry Into the Geographical Ranges of Species in that Quarter of the Globe, Published Under the Authority of the Lords Commissioners of Her Majesty’s Treasury, Invertebratae’. (Ed. A. Smith.) pp. 53–71, pls 2, 3. (Smith, Elder & Co.: London.)
Milne Edwards, H. (1837). ‘Histoire Naturelle des Crustacés, Comprenant l’Anatomie, la Physiologie et la Classification de ces Animaux. Vol. 2.’ pp. 1–532. Atlas: 32 pp, pls 1–14, 14 bis, 15–25 bis, 26–42. (Roret: Paris.)
Milne Edwards, H. (1852). De la famille des ocypodides (Ocypodidae). Second mémoire. In ‘Observations sur les Affinités Zoologiques et la Classification Naturelle des Crustacés’. [Annales des Sciences Naturelles Paris (Zoology) 18, 128–166, pls 3, 4.]
Milne Edwards, H. (1853). Mémoire sur la famille des Ocypodides. Suite (1). Deuxiéme tribu principale. Annales des Sciences Naturelles, Comprenant la Zoologie, la Botanique, l’Anatomie et la Physiologie Comparées des Deux Régnes et l’Histoire des Corps Organisés Fossiles, Librairie de Victor Masson, Paris, Series 3, Zoology 20, 163–228, pls 6–11.
Milne-Edwards, A. (1867). Descriptions des quelques espèces nouvelles de Crustacés, Brachyures. Annales de la Société Entomologique de France, Series 4 7, 263–288.
Naruse, T., and Clark, P. F. (2009). Establishment of a new genus for Asthenognathus gallardoi Serène & Soh, 1976 within Gaeticinae Davie & N.K. Ng, 2007 (Crustacea: Decapoda: Brachyura: Varunidae). Zootaxa 1987, 61–68.
Naruse, T., Fujita, Y., and Ng, P. K. L. (2009). A new genus and new species of commensal crab (Crustacea: Brachyura: Pinnotheroidea) from Oura Bay, Okinawa Island, Japan. Zootaxa 2053, 59–68.
Ng, N. K., Davie, P. J. F., Schubart, C. D., and Ng, P. K. L. (2007). Xenograpsidae, a new family of grapsoid crabs (Crustacea: Brachyura) associated with shallow water hydrothermal vents. Raffles Bulletin of Zoology 16, 233–256.
Ng, N. K., Huang, J.-F., and Ho, P.-H. (2000). Description of a new species of hydrothermal crab, Xenograpsus testudinatus (Crustacea: Decapoda: Brachyura: Grapsidae) from Taiwan. National Taiwan Museum Special Publication Series 10, 191–199.
Ng, P. K. L., and Clark, P. F. (2014). Selwynia, a senior synonym of Aphanodactylus, with a redescription of Selwynia laevis (Crustacea: Brachyura: Pinnotheroidea: Aphanodactylidae). Marine Biology Records 7, e113.
| Selwynia, a senior synonym of Aphanodactylus, with a redescription of Selwynia laevis (Crustacea: Brachyura: Pinnotheroidea: Aphanodactylidae).Crossref | GoogleScholarGoogle Scholar |
Ng, P. K. L., and Rahayu, D. L. (2016). On the genera Selwynia Borradaile, 1903, and Gandoa Kammerer, 2006, with descriptions of two new species from Papua New Guinea and French Polynesia (Crustacea: Decapoda: Brachyura: Aphanodactylidae). Zootaxa 4092, 339–370.
| On the genera Selwynia Borradaile, 1903, and Gandoa Kammerer, 2006, with descriptions of two new species from Papua New Guinea and French Polynesia (Crustacea: Decapoda: Brachyura: Aphanodactylidae).Crossref | GoogleScholarGoogle Scholar |
Ng, P. K. L., Ahyong, S. T., and Komai, T. (2010). On the male of Aphanodactylus loimiae Konishi & Noda, 1999 (Crustacea: Brachyura: Pinnotheroidea: Aphanodactylidae). The Raffles Bulletin of Zoology 58, 75–78.
Ng, P. K. L., Guinot, D., and Davie, P. J. F. (2008). Systema Brachyuorum: Part I. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology 17, 1–286.
Ng, P. K. L., Rahayu, D. L., and Shih, H.-T. (2016). Ankerius aenigmaticus, a new genus and new species of aphanodactylid crab symbiotic with polychaetes from the Red Sea coast of Saudi Arabia (Crustacea: Decapoda: Brachyura: Aphanodactylidae). Zootaxa 4179, 271–278.
| Ankerius aenigmaticus, a new genus and new species of aphanodactylid crab symbiotic with polychaetes from the Red Sea coast of Saudi Arabia (Crustacea: Decapoda: Brachyura: Aphanodactylidae).Crossref | GoogleScholarGoogle Scholar |
Page, R. D. M. (1983). Description of a new species of Pinnotheres, and redescription of P. novaezelandiae (Brachyura: Pinnotheridae). New Zealand Journal of Zoology 10, 151–162.
| Description of a new species of Pinnotheres, and redescription of P. novaezelandiae (Brachyura: Pinnotheridae).Crossref | GoogleScholarGoogle Scholar |
Palacios-Theil, E., Cuesta, J. A., Campos, E., and Felder, D. L. (2009). Molecular genetic re-examination of subfamilies and polyphyly in the family Pinnotheridae (Crustacea: Decapoda). In ‘Decapod Crustacean Phylogenetics. Crustacean Issues 18’. (Eds J. W. Martin, K. A. Crandall, and D. L. Felder.) pp. 457–474. (CRC Press, Taylor & Francis Group: Boca Raton, FL.)
Palacios Theil, E., Cuesta, J. A., and Felder, D. L. (2016). Molecular evidence for non-monophyly of the pinnotheroid crabs (Crustacea: Brachyura: Pinnotheroidea), warranting taxonomic reappraisal. Invertebrate Systematics 30, 1–27.
| Molecular evidence for non-monophyly of the pinnotheroid crabs (Crustacea: Brachyura: Pinnotheroidea), warranting taxonomic reappraisal.Crossref | GoogleScholarGoogle Scholar |
Pallas, S. P. (1772). ‘Spicilegia Zoologica. Quibus Novae Imprimis et Obscurae Animalium Species Iconibus Descriptionibus Atque Commentariis Illustrantor.’ 9, 81–84, pl. 5, figs 7, 8.
Paul’son, O. (1875). ‘Studies on Crustacea of the Red Sea With Notes Regarding Other Seas. Part 1 Podophthalmata and Edriophthalmata (Cumacea).’ pp. i–xiv, 1–144, pls 1–22. (Kiev) [In Russian]
Pocock, R. I. (1889). On the Arachnida, Myriopoda and Land-Crustacea of Christmas Island. Proceedings of the Zoological Society of London 1888(IV), 556–564, figs 1, 2.
Poeppig, E. (1836). Crustacea chilensia nova aut minus nota descripsit. Archiv für Naturgeschichte 2, 134–144, pl. 4.
Pohle, G., and Marques, F. (1998). Phylogeny of the Pinnotheridae: larval and adult evidence, with emphasis on the evolution of gills. Invertebrate Reproduction & Development 33, 229–239.
| Phylogeny of the Pinnotheridae: larval and adult evidence, with emphasis on the evolution of gills.Crossref | GoogleScholarGoogle Scholar |
Rafinesque, C. S. (1815). ‘Analyse de la Nature, ou Tableau de l’Univers et des Corps Organisés.’ (L’Imprimerie de Jean Barravecchia: Palermo.)
Rambaut, A., and Drummond, A. J. (2007). Tracer v1.4. Available at http://beast.bio.ed.ac.uk/Tracer
Rathbun, M. J. (1898). The Brachyura collected by the U.S. Fish Commission steamer Albatross on the voyage from Norfolk, Virginia, to San Francisco, California, 1887–1888. Proceedings of the United States National Museum 21, 567–616, pls 41–44.
Rathbun, M. J. (1918). The grapsoid crabs of America. Bulletin of the United States National Museum 97, 1–461, pls 1–161.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hōhna, 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.
Schmitt, W. L., McCain, J. C., and Davidson, E. (1973). ‘Decapoda I. Brachyura I. Fam. Pinnotheridae.’ Crustaceorum Catalogus pars 3, pp. 1–160. (W. Junk: The Hague, Netherlands.)
Schubart, C. D., Cannicci, S., Vannini, M., and Fratini, S. (2006). Molecular phylogeny of grapsoid crabs (Decapoda, Brachyura) and allies based on two mitochondrial genes and a proposal for refraining from current superfamily classification. Journal of Zoological Systematics and Evolutionary Research 44, 193–199.
| Molecular phylogeny of grapsoid crabs (Decapoda, Brachyura) and allies based on two mitochondrial genes and a proposal for refraining from current superfamily classification.Crossref | GoogleScholarGoogle Scholar |
Schubart, C. D., and Cuesta, J. A. (2010). Phylogenetic relationships of the Plagusiidae Dana, 1851 (Brachyura), with description of a new genus and recognition of Percnidae Števčić, 2005, as an independent family. Studies on Brachyura: a homage to Danièle Guinot. Crustaceana Monographs 11, 279–299.
Schubart, C. D., Cuesta, J. A., Diesel, R., and Felder, D. L. (2000). 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=34fadd34925f9d3d1f66f0784e5f1190CAS |
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 |
Shen, C.-J. (1930). A new Scopimera from North China. Bulletin of Fan Memorial Institute of Biology 1, 227–233.
Shih, H.-T., Ng, P. K. L., Davie, P. J. F., Schubart, C. D., Türkay, M., Naderloo, R., Jones, D., and Liu, M.-Y. (2016). Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. The Raffles Bulletin of Zoology 64, 139–175.
Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Systematic Biology 51, 492–508.
| An approximately unbiased test of phylogenetic tree selection.Crossref | GoogleScholarGoogle Scholar |
Shimodaira, H., and Hasegawa, M. (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246–1247.
| CONSEL: for assessing the confidence of phylogenetic tree selection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FgtFOlsw%3D%3D&md5=1d0bf48fd7d71f08254469bc19acc8ecCAS |
Simon, C., Frati, 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.
| Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=50ad7fcc61dab51d38e3ca77bd6f77c1CAS |
Smith, S. I. (1870). Ocypodoidea. Notes on North American Crustacea, I. Transactions of the Connecticut Academy of Sciences 2, 113–176.
| Ocypodoidea. Notes on North American Crustacea, I.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.
| 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=bf1c47d07b064fc1a91a82830ae5d513CAS |
Stimpson, W. (1858). Crustacea Ocypodoidea. Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republica Federata missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars V. Proceedings. Academy of Natural Sciences of Philadelphia 10, 93–110.
Tesch, J. J. (1918). ‘Decapoda Brachyura II. Goneplacidae and Pinnotheridae.’ Siboga Expeditie Monographie Vol. 39c1. pp. 149–295. (E.J. Brill: Leiden.)
Tsang, L. M., Chan, B. K. K., Shih, F.-L., Chu, K. H., and Chen, A. C.-L. (2009). Host associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pygomatidae) inhabiting the Millepora coral. Molecular Ecology 18, 1463–1475.
Tsang, L. M., Schubart, C. D., Ahyong, S. T., Lai, J. C. Y., Au, E. Y. C., Chan, T. Y., Ng, P. K. L., and Chu, K. H. (2014). Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs. Molecular Biology and Evolution 31, 1173–1187.
| Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFCis7o%3D&md5=587a67d04a4acce20aeeaff1264d62adCAS |
van der Meij, S. E. T., and Schubart, C. D. (2014). Monophyly and phylogenetic origin of the gall crab family Cryptochiridae. Invertebrate Systematics 28, 491–500.
| Monophyly and phylogenetic origin of the gall crab family Cryptochiridae.Crossref | GoogleScholarGoogle Scholar |
Wada, K., and Sakai, K. (1989). A new species of Macrophthalmus closely related to M. japonicus (de Haan) (Crustacea, Decapoda, Ocypodidae). Senckenbergiana Maritima 20, 131–146.