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

Molecular phylogeny of the crab genus Metopograpsus H. Milne Edwards, 1853 (Decapoda : Brachyura : Grapsidae) reveals high intraspecific genetic variation and distinct evolutionarily significant units

S. Fratini A B E , S. Cannicci A C and C. D. Schubart D
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of Florence, via Madonna del Piano 6, Sesto Fiorentino, Italy.

B Mangrove Specialist Group, IUCN Species Survival Commission, 28 rue Mauverney, CH-1196 Gland, Switzerland.

C The Swire Institute of Marine Science and the School of Biological Sciences, The University of Hong Kong, Hong Kong, Special Administrative Region, P.R. China.

D Zoologie & Evolution, Universität Regensburg, D-93040 Regensburg, Germany.

E Corresponding author. Email: sarafratini@unifi.it

Invertebrate Systematics 32(1) 215-223 https://doi.org/10.1071/IS17034
Submitted: 5 April 2017  Accepted: 5 July 2017   Published: 2 February 2018

Abstract

The Indo-Pacific genus Metopograpsus belongs to the family Grapsidae and comprises six species of intertidal crabs inhabiting sheltered rocky shores and mangrove forests. All species are opportunistic feeders and four of them are associated with roots and trunks of mangroves. So far, no comprehensive molecular phylogenetic study has been conducted on this genus, despite the fact that some species are not easily separable from a morphological point of view. We performed a phylogenetic and phylogeographic investigation based on sequences corresponding to both ribosomal mitochondrial DNA genes from 44 samples of Metopograpsus spp., covering the distribution ranges of each species. Our main aims were to validate species identification across their respective distribution ranges and depict the phylogeographic patterns within each species. Our phylogenetic inference reconstructions confirmed monophyly of the six species. We also recorded a high intraspecific genetic variation and strong phylogeographic structure within M. thukuhar and M. quadridentatus. This indicates the occurrence of distinct evolutionarily significant units within these two taxa, possibly corresponding to undescribed species. Further nuclear DNA-based phylogeographic analyses, as well as morphological investigations, will be necessary to assign a taxonomic value to the recorded evolutionarily significant units.

Additional keywords: Crustacea, Indo-Pacific, mangrove crabs, phylogeny, phylogeography.


References

Al-Ghais, S. M., and Cooper, R. T. (1996). Brachyura (Grapsidae, Ocypodidae, Portunidae, Xanthidae and Leucosiidae) of Umm Al Quwain mangal, United Arab Emirates. Tropical Zoology 9, 409–430.
Brachyura (Grapsidae, Ocypodidae, Portunidae, Xanthidae and Leucosiidae) of Umm Al Quwain mangal, United Arab Emirates.Crossref | GoogleScholarGoogle Scholar |

Anger, K. (2001). The biology of decapod crustacean larvae. In ‘Crustacean Issues. Vol. 14’. (Ed. A. A. Balkema.) (Lisse: The Netherlands.)

Banerjee, S. K. (1960). Biological results of the Snellius Expedition XVIII. The genera Grapsus, Geograpsus, and Metopograpsus (Crustacea Brachyura). Temminckia 10, 132–199.

Benzie, J. A., Ballment, E., Forbes, A. T., Demetriades, N. T., Sugama, K., Haryanti, , and Moria, S. (2002). Mitochondrial DNA variation in Indo-Pacific populations of the giant tiger prawn, Penaeus monodon. Molecular Ecology 11, 2569.
| 1:CAS:528:DC%2BD38Xpsl2msLw%3D&md5=04fe22fab8866f1d64e16b895c7141c1CAS |

Borsa, P., Durand, J.-D., Chen, W.-J., Hubert, N., Muths, D., Mou-Tham, G., and Kulbicki, M. (2016). Comparative phylogeography of the western Indian Ocean reef fauna. Acta Oecologica – International Journal of Ecology 72, 72–86.
Comparative phylogeography of the western Indian Ocean reef fauna.Crossref | GoogleScholarGoogle Scholar |

Bowen, B. W., Gaithen, M. R., DiBattista, J. D., Iacchei, M., Andrews, K. R., Grant, W. S., Toonen, R. J., and Briggs, J. C. (2016). Comparative phylogeography of the ocean planet. Proceedings of the National Academy of Sciences of the United States of America 113, 7962–7969.
Comparative phylogeography of the ocean planet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFOku7bM&md5=ceca5598996a3b6c2bc4f29cddd6de75CAS |

Carpenter, K. E., Barber, P. H., Crandall, E. D., Ablan-Lagman, M. C. A., Ambariyanto, G., Mahardika, G. N., Manjaji-Matsumoto, B. M., Juinio-Menez, M. A., Santos, M. D., Starger, C. J., and Toha, A. H. A. (2011). Comparative phylogeography of the Coral Triangle and implications for marine management. Journal of Marine Biology 396982, .
Comparative phylogeography of the Coral Triangle and implications for marine management.Crossref | GoogleScholarGoogle Scholar |

Chappell, J., and Shackleton, N. J. (1986). Oxygen isotopes and sea level. Nature 324, 137–140.
Oxygen isotopes and sea level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXptVyq&md5=e0961cf9904434503b7387bfb5ca028eCAS |

Christy, J. H. (2011). Timing of hatching and release of larvae by brachyuran crabs: patterns, adaptive significance and control. Integrative and Comparative Biology 51, 62–72.
Timing of hatching and release of larvae by brachyuran crabs: patterns, adaptive significance and control.Crossref | GoogleScholarGoogle Scholar |

Crosnier, A. (1965). Crustacés Dècapodes. Grapsidae et Ocypodidae. Faune de Madagascar 18, 1–143.

Cuesta, J. A., Guerao, G., Schubart, C. D., and Anger, K. (2011). Morphology and growth of the larval stages of Geograpsus lividus (Crustacea, Brachyura), with the descriptions of new larval characters for the Grapsidae and an undescribed setation pattern in extended developments. Acta Zoologica 92, 225–240.
Morphology and growth of the larval stages of Geograpsus lividus (Crustacea, Brachyura), with the descriptions of new larval characters for the Grapsidae and an undescribed setation pattern in extended developments.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.
| 1:CAS:528:DC%2BC38XhtFagu7fO&md5=7bdb4f2b26d240256a0aac67a36902f8CAS |

Farris, J. S., Källersjäö, M., Kluge, A.G., and Bult, C. (1995). Testing significance of incongruence. Cladistics 10, 315–319.

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.

Fielder, D. R., and Greenwood, J. G. (1983). The complete larval development of Metopograpsus frontalis Miers (Decapoda, Grapsidae), reared in the laboratory. Proceedings of the Royal Society of Queensland 94, 51–60.

Forest, J., and Guinot, D. (1961). Crustaces decapodes brachyoures de Tahiti et des Taunioto. In ‘Expedition Française sur les Reclis Coralliens de la Nouvelle Caledonie’. pp. 1–195. (Editions de la Fondation Singer-Polignac: Paris.)

Fratini, S., Cannicci, S., Abincha, L., and Vannini, M. (2000). Feeding, temporal and spatial preferences of Metopograpsus thukuhar (Decapoda; Grapsidae): an opportunistic mangrove dweller. Journal of Crustacean Biology 20, 326–333.
Feeding, temporal and spatial preferences of Metopograpsus thukuhar (Decapoda; Grapsidae): an opportunistic mangrove dweller.Crossref | GoogleScholarGoogle Scholar |

Fratini, S., Vannini, M., Cannicci, S., and Schubart, C. D. (2005). Tree-climbing mangrove crabs, a case of convergent evolution. Evolutionary Ecology Research 7, 219–233.

Gordon, A. L., and Fine, R. A. (1996). Pathways of water between the Pacific and Indian oceans in the Indonesian seas. Nature 379, 146–149.
Pathways of water between the Pacific and Indian oceans in the Indonesian seas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xkt1eitQ%3D%3D&md5=08b49d0dc230d6fb146fd4b5593c3fd5CAS |

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.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=51032c35c9b55c2e0a0ae6daa653f17bCAS |

Hartnoll, R. G. (1975). Grapsidae and Ocypodidae (Decapoda: Brachyura) of Tanzania. Journal of Zoology 177, 305–328.
Grapsidae and Ocypodidae (Decapoda: Brachyura) of Tanzania.Crossref | GoogleScholarGoogle Scholar |

Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
Dating of the human–ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=c8be9bbf5429b35952e43b97d49562acCAS |

Ip, B. H. Y., Schubart, C. D., Tsang, L. M., and Chu, K. H. (2015). Phylogeny of the shore crab family Grapsidae (Decapoda: Brachyura: Thoracotremata) based on a multilocus approach. Zoological Journal of the Linnean Society 174, 217–227.
Phylogeny of the shore crab family Grapsidae (Decapoda: Brachyura: Thoracotremata) based on a multilocus approach.Crossref | GoogleScholarGoogle Scholar |

Kakati, V. S. (1982). Larval development of the Indian grapsid crab, Metopograpsus latifrons H. Milne Edwards in vitro. Indian Journal of Marine Sciences 2, 311–316.

Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=923eb8b83abb772e70745a603d99fa8fCAS |

Kirkendale, L. A., and Meyer, C. P. (2004). Phylogeography of the Patelloida profunda group (Gastropoda: Lottidae): diversification in a dispersal-driven marine system. Molecular Ecology 13, 2749–2762.
| 1:CAS:528:DC%2BD2cXotlemurg%3D&md5=2e420956a1782105d901f0c6532a41ffCAS |

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.

Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
| 1:CAS:528:DC%2BD2cXntFGqu7s%3D&md5=2cfbf7ebbf7aee116760c97f3e0d9d48CAS |

Lai, J. C. Y., Ng, P. K. L., and Davie, P. J. F. (2010). A revision of the Portunus pelagicus species complex (Crustracea: Brachyura: Portunidae), with the recognition of four species. The Raffles Bulletin of Zoology 58, 199–237.

Levin, L. A. (2006). Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46, 282–297.
Recent progress in understanding larval dispersal: new directions and digressions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFehsLw%3D&md5=1485f64e7fe0038bb802299ffa319dfdCAS |

Liu, J. Y. [Ruiyu] (Ed.) (2008). ‘Checklist of Marine Biota of China seas.’ (China Science Press.)

Masagca, J. T. (2011). Occurrence of arboreal-climbing grapsids and other brachyurans in two mangrove areas of southern Luzon, Philippines. Biotropica 18, 61–73.

Moritz, C. (1994). Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution 9, 373–375.
| 1:STN:280:DC%2BC3M7itFWhsA%3D%3D&md5=3c5716803b4327293b8ecc03ed168fa3CAS |

Ng, P. K. L, Guinot, D., and Davie, P. J. F. (2008). Systema Brachyurorum: Part I. An annoted checklist of extant Brachyuran crabs of the world. The Raffles Bulletin of Zoology 17, 1–286.

Palumbi, S., Martin, A., Romano, S., McMillan, O. W., Stice, L., and Grabowski, G. (1991). ‘The Simple Fool’s Guide to PCR.’ (Department of Zoology and Kewalo Marine Laboratory, University of Hawaii: Honolulu.)

Pasupathi, K., and Kannupandi, T. (1986). Laboratory reared larval stages of the mangrove grapsid crab, Metopograpsus maculatus H Milne-Edwards. Mahasagar 19, 233–244.

Patarnello, T., Volckaert, F. A. M., and Castilho, R. (2007). Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographic break? Molecular Ecology 16, 4426–4444.
Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographic break?Crossref | GoogleScholarGoogle Scholar |

Paulay, G. (2007). Metopograpsus oceanicus (Crustacea: Brachyura) in Hawaii and Guam: another recent invasive? Pacific Science 61, 295–300.
Metopograpsus oceanicus (Crustacea: Brachyura) in Hawaii and Guam: another recent invasive?Crossref | GoogleScholarGoogle Scholar |

Poon, D. Y. N., Cheb, B. K. K., and Williams, G. A. (2010). Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) and Perisesarma bidens (Sesarmidae): implications for mangrove food webs. Hydrobiologia 638, 29–40.
Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) and Perisesarma bidens (Sesarmidae): implications for mangrove food webs.Crossref | GoogleScholarGoogle Scholar |

Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=aafbf462d9871e9c06a8a479b904d2a8CAS |

Ragionieri, L., Fratini, S., Vannini, M., and Schubart, C. D. (2009). Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Molecular Phylogenetics and Evolution 52, 825–834.
| 1:CAS:528:DC%2BD1MXosVaqtbs%3D&md5=3d33b952b32d547ba2bd63f37623c75eCAS |

Ragionieri, L., Fratini, S., and Schubart, C. D. (2012). Revision of the Neosarmatium meinerti species complex (Decapoda: Brachyura: Sesarmidae), with descriptions of three pseudocryptic Indo-West Pacific species. The Raffles Bulletin of Zoology 60, 71–87.

Schubart, C. D. (2009). Mitochondrial DNA and decapod phylogenies: the importance of pseudogenes and primer optimization. In ‘Crustacean Issues 18: Decapod Crustacean Phylogenetics’. (Eds J. W. Martin, K. A. Crandall and D. L. Felder.) pp. 47–65. (Taylor & Francis/CRC Press: Boca Raton, FL.)

Schubart, C. D. (2011). Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-Atlantic gene flow based on mtDNA. Zoologischer Anzeiger 250, 472–478.
Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-Atlantic gene flow based on mtDNA.Crossref | GoogleScholarGoogle Scholar |

Schubart, C. D., Neigel, J. E., and Felder, D. L. (2000). The use of the mitochondrial 16S rRNA gene for phylogenetic and biogeographic studies of Crustacea. In ‘The Biodiversity Crisis and Crustacea. Proceedings of the Fourth International Crustacean Congress, Amsterdam, Netherlands, 20–24 July 1998’. Vol. 2. Crustacean Issues 12, 817–830.

Schubart, C. D., Cannicci, S., Vannini, M., and Fratini, S. (2006). Molecular phylogeny of grapsoid crabs from East Africa 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 from East Africa based on two mitochondrial genes and a proposal for refraining from current superfamily classification.Crossref | GoogleScholarGoogle Scholar |

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 |

Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods).’ (Sinauer Associates: Sunderland, MA.)

Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.
| 1:CAS:528:DyaK3sXks1CksL4%3D&md5=26e2ce3e1989cd2013ede7773772429fCAS |

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 origins of freshwater crabs. Molecular Biology and Evolution 31, 1173–1187.
Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origins of freshwater crabs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFCis7o%3D&md5=587a67d04a4acce20aeeaff1264d62adCAS |

Turner, E. (1992). A northern Pacific seastar, Asterias amurensis, in Tasmania. AMSA Bulletin 120, 18–19.

Tweedie, M. W. F. (1949). The species of Metopograpsus (Crustacea, Brachyura). Bijdragen tot de Dierkunde 28, 466–471.

Vannini, M., Oluoch, A., and Ruwa, R. K. (1997). The tree-climbing crabs of Kenyan mangroves. In ‘Mangrove Ecosystem Studies in Latin America and Africa’. (Eds B. Kjerfve, B. L. De Lacerda and E. S. Diop.) pp. 325–338. UNESCO Technical Papers in Marine Sciences. (UNESCO: Paris.)

von Hagen, H. O. (1977). The tree climbing crabs of Trinidad. Studies on the Fauna Curaçao 54, 25–59.

Ward, R. D., and Andrew, J. (1995). Population genetics of the northern Pacific seastar Asterias amurensis (Echinodermata: Asteriidae): allozyme differentiation among Japanese, Russian, and recently introduced Tasmania populations. Marine Biology 124, 99–109.
Population genetics of the northern Pacific seastar Asterias amurensis (Echinodermata: Asteriidae): allozyme differentiation among Japanese, Russian, and recently introduced Tasmania populations.Crossref | GoogleScholarGoogle Scholar |

Wiens, J. J. (2006). Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39, 34–42.
Missing data and the design of phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVGgsQ%3D%3D&md5=04580ceb9771177bb9e56d1bb557e201CAS |

Williams, S. T., Jara, J., Gomez, E., and Knowlton, N. (2002). The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integrative and Comparative Biology 42, 941–952.
The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnhtlGmtQ%3D%3D&md5=8c8518722ce7186ce838b90d7f89ab52CAS |

Wilson, B. (2013). ‘The Biogeography of the Australian North West Shelf. Environmental Change and Life’s Response.’ (Elsevier.)

Yamindago, A., Senanan, W., and Tangkrock-Olan, N. (2013). Verification on morphological identification of grapsid crabs genus Metopograpsus H. Milne Edwards, 1853 from Chon Buri Province using partial sequences of mitochondrial 16S rRNA, 12S rRNA and cytochrome c oxidase subunit I (COI) genes. Burapha Science Journal 18, 181–193.

Yang, L., Tan, Z., Wang, D., Xue, L., Guan, M.-X., Huang, T., and Li, R. (2014). Species identification through mitochondrial rRNA genetic analysis. Scientific Reports 4, 4089.
Species identification through mitochondrial rRNA genetic analysis.Crossref | GoogleScholarGoogle Scholar |