Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T15:33:48.609Z Has data issue: false hasContentIssue false

Molecular phylogeny of enigmatic Caribbean spider crabs from the Mithrax–Mithraculus species complex (Brachyura: Majidae: Mithracinae): ecological diversity and a formal test of genera monophyly

Published online by Cambridge University Press:  23 November 2009

J. Antonio Baeza*
Affiliation:
Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancón, Republic of Panama Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, FL 34949, USA
Juan A. Bolaños
Affiliation:
Grupo de Investigación en Carcinología, Escuela de Ciencias Aplicadas del Mar, Núcleo Nueva Esparta, Universidad de Oriente, Isla Margarita, Venezuela
Soledad Fuentes
Affiliation:
NOAA Fisheries, Milford Laboratory, 212 Rogers Avenue, Milford CT 06460, USA
Jesús E. Hernandez
Affiliation:
Grupo de Investigación en Carcinología, Escuela de Ciencias Aplicadas del Mar, Núcleo Nueva Esparta, Universidad de Oriente, Isla Margarita, Venezuela
Carlos Lira
Affiliation:
Grupo de Investigación en Carcinología, Escuela de Ciencias Aplicadas del Mar, Núcleo Nueva Esparta, Universidad de Oriente, Isla Margarita, Venezuela
Régulo López
Affiliation:
Grupo de Investigación en Carcinología, Escuela de Ciencias Aplicadas del Mar, Núcleo Nueva Esparta, Universidad de Oriente, Isla Margarita, Venezuela
*
Correspondence should be addressed to: J.A. Baeza, Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancón, Republic of Panama email: baezaa@si.edu

Abstract

Crabs from the Mithrax–Mithraculus species complex are known for their diversity of lifestyles, habitats, and coloration. This group includes small, colourful, symbiotic species and much larger, reef-dwelling crabs targeted by fishermen. The evolutionary relationships between the species within this complex are not well-defined. Previous studies based upon morphological characters have proposed the separation of this complex into two genera (Mithrax and Mithraculus), but cladistic analyses based upon larval characters do not support this division. A molecular phylogeny of the group may help to resolve this long-standing taxonomic question and shed light on the ecological conditions driving the diversity of these crabs. Using a 550-bp alignment of the 16S rRNA mitochondrial DNA segment we examined the phylogenetic relationships between 8 species within the Mithrax–Mithraculus complex native to the Caribbean. The resulting phylogeny indicates that this complex is paraphyletic, as it includes the genus Microphrys. The analyses revealed a well-supported, monophyletic group containing four species of Mithraculus (M. cinctimanus, M. coryphe, M. sculptus and M. forceps) and supported one pair of sister species from the genus Mithrax (M. caribbaeus and M. spinosissimus). No complete segregation of species, according to genera, was evident, however, from tree topologies. Bayesian-factor analyses revealed strong support for the unconstrained tree instead of alternative trees in which monophyly of the two genera was forced. Thus, the present molecular phylogeny does not support the separation of the species within this complex into the genera Mithrax and Mithraculus. A review of the literature demonstrated considerable phenotypic variation within monophyletic clades in this group.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abele, L. and Kim, W. (1986) An illustrated guide to the marine decapod crustaceans of Florida. Tallahassee: Department of Environmental Regulation.Google Scholar
Ahyong, S.T. and O'Meally, D. (2004) Phylogeny of the Decapoda Reptantia: resolution using three molecular loci and morphology. Raffles Bulletin of Zoology 52, 673693.Google Scholar
Ahyong, S.T., Lai, J.C.Y., Sharkey, D., Colgan, D.J. and Ng, P.K.L. (2007) Phylogenetics of the brachyuran crabs (Crustacea: Decapoda): the status of Podotremata based on small subunit nuclear ribosomal RNA. Molecular Phylogenetics and Evolution 45, 576586.CrossRefGoogle ScholarPubMed
Baeza, J.A., Thiel, M. and Stotz, W. (2001) The life history of Allopetrolisthes spinifrons, a crab associate of the sea anemone Phymactis clematis. Journal of the Marine Biological Association of the United Kingdom 81, 6976.CrossRefGoogle Scholar
Baeza, J.A. and Thiel, M. (2007) The mating system of symbiotic crustaceans. A conceptual model based on optimality and ecological constraints. In Duffy, J.E. and Thiel, M. (eds) Reproductive and social behaviour: crustaceans as model systems. Oxford: Oxford University Press, pp. 245255.Google Scholar
Baeza, J.A., Schubart, C.D., Zillner, P., Fuentes, S. and Bauer, R.T. (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and pair-living. Biological Journal of the Linnean Society 96, 415424.CrossRefGoogle Scholar
Bermingham, E., McCafferty, S.S. and Martin, A.P. (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian isthmus. In Kocher, T.D. and Stepien, C.A. (eds) Molecular systematics of fishes. San Diego: Academic Press, pp. 113128.Google Scholar
Bolaños, J.A. and Scelzo, M.A. (1981) Larval development of the spider crab Mithrax verrucosus Milne-Edwards, reared in the laboratory (Decapoda: Brachyura: Majidae). The American Zoologist 21, 989.Google Scholar
Bolaños, J.A., Lares, L.B. and Hernández, J.E. (1990) Desarrollo larval de Mithrax caribbaeus Rathbun, 1920 (Crustacea: Decapoda: Majidae) realizado en condiciones de laboratorio. Boletín del Instituto Oceanográfico de Venezuela 29, 6789.Google Scholar
Bolaños, J.A., Hernández, G. and Lira, C. (2000) Mithraculus cinctimanus Stimpson, 1860 y Speloeophorus pontifer (Stimpson, 1871) (Crustacea: Decapoda: Brachyura), dos nuevas adiciones a la carcinofauna venezolana. Boletín del Instituto Oceanográfico de Venezuela 39, 2531.Google Scholar
Boschi, E. (2000) Species of decapod crustaceans and their distribution in the American marine zoogeographic province. Revista de Investigación y Desarrollo Pesquero 13, 7136.Google Scholar
Fransozo, A. and Hebling, N.J. (1982) Desenvolvimento potsembrionario de Mithrax hispidus (Herbst, 1790) (Decapoda, Majidae) em laboratorio. Ciência e Cultura 34, 385395.Google 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, 219233.Google Scholar
Goy, J.W., Bookhout, C.G. and Costlow, J.D. Jr (1981) Larval development of the spider crab Mithrax pleuracanthus Stimpson reared in laboratory (Decapoda: Brachyura: Majidae). Journal of Crustacean Biology 1, 5162.Google Scholar
Huelsenbeck, J.P. (2000) MrBayes: Bayesian Inferences of Phylogeny (software). New York: University of Rochester Press.Google Scholar
Hultgren, K. and Stachowicz, J.J. (2008) Molecular phylogeny of the brachyuran crab superfamily Majoidea indicates close congruence with larval morphology-based trees. Molecular Phylogenetics and Evolution 48, 986996.CrossRefGoogle Scholar
Hultgren, K. and Stachowicz, J.J. (2009) Evolution of decoration in majoid crabs: a comparative phylogenetic analysis of the role of body size and alternative defensive strategies. The American Naturalist 173, 566578.Google Scholar
Kass, R.E. and Raftery, A.E. (1995) Bayes factors. Journal of the American Statistical Association 90, 773795.Google Scholar
Lessios, H.A. (2008) The great American schism: divergence of marine organisms after the rise of the Central American isthmus. Annual Review of Ecology and Systematics 39, 6391.CrossRefGoogle Scholar
Manning, R.B. (1970) Mithrax (Mithraculus) commensalis, a new West Indian spider crab (Decapoda, Majidae) commensal with a sea anemone. Crustaceana 19, 157161.Google Scholar
Marques, F.P.L., Pohle, G.W. and Vrbova, L. (2003) On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), and a review of Mithracine phylogenetic aspects. Journal of Crustacean Biology 23, 187200.Google Scholar
Martin, J.W. and Davis, G.E. (2001) An updated classification of the Recent Crustacea. Natural History Museum of L.A. County, Science Series 39, 1124.Google Scholar
Melo, G.A.S. (1996) Manual de identificação dos Brachyura (Caranguejos e Siris) do litoral brasileiro, São Paulo, Brasil. São Paulo: Editora Plêiade.Google Scholar
Ng, P.K.L., Guinot, D. and Davie, P.J.F. (2008) Systema Brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bulletin of Zoology 17, 1286.Google Scholar
Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P. and Nieves-Aldrey, J.L. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 4767.CrossRefGoogle ScholarPubMed
Palumbi, S.R., Martin, A., Romano, S., Mcmillan, W.O., Stice, L. and Grabowski, G. (1991) The simple fool's guide to PCR. A collection of PCR protocols. Honolulu: University of Hawaii.Google Scholar
Pohle, G.W. and Marques, F.P.L. (2000) Larval stages of Paradasygius depressus (Bell, 1835) (Brachyura: Majidae) and a phylogenetic hypothesis for 21 genera of Majidae. Proceedings of the Biological Society of Washington 113, 739760.Google Scholar
Porter, M.L., Perez-Losada, M. and Crandall, K.A. (2005) Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution 37, 355369.Google Scholar
Posada, D. and Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.Google Scholar
Provenzano, A.J. and Brownell, W.N. (1977) Larval and early post-larval stages of the west Indian spider crab, Mithrax spinosissimus (Lamarck) (Decapoda: Majidae). Proceedings of the Biological Society of Washington 90, 735752.Google Scholar
Rathbun, M.J. (1925) The spider crabs of America. Bulletin of the United States National Museum 129, 1613.Google Scholar
Rhyne, A.L., Fujita, Y. and Calado, R. (2004) Larval development and 1st crab of Mithraculus sculptus (Decapoda: Brachyura: Majoidea: Mithracidae) described from laboratory-reared material. Journal of the Marine Biological Association of the United Kingdom 86, 11331147.Google Scholar
Rodríguez, G. (1980) Crustáceos decápodos de Venezuela. Caracas: IVIC.Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.Google Scholar
Santana, W., Pohle, G. and Marques, F. (2003) Zoeal stages and megalopa of Mithrax hispidus (Herbst, 1790) (Decapoda: Brachyura: Majoidea: Mithracidae): a reappraisal of larval characters from laboratory cultured material and a review of larvae of the Mithrax–Mithraculus species complex. Invertebrate Reproduction and Development 44, 1732.CrossRefGoogle Scholar
Santana, W., Marques, F. and Pohle, G. (2004) Larval stages of Stenocionops furcatus (Olivier, 1791) (Decapoda: Brachyura: Majoidea) and a reappraisal of larval morphological characters for Mithracidae. Journal of Plancton Research 26, 859874.Google Scholar
Scholtz, G. and Richter, S. (1995) Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca). Zoological Journal of the Linnean Society 113, 289328.CrossRefGoogle Scholar
Scotto, L.E. and Gore, R.H. (1980) Larval development under laboratory conditions of the tropical spider crab Mithrax (Mithraculus) coryphe (Herbst, 1801) (Brachyura: Majidae). Proceedings of the Biological Society of Washington 93, 551562.Google Scholar
Schubart, C.D., Diesel, R. and Hedges, S.B. (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393, 363365.Google Scholar
Schubart, C.D., Neigel, J.E. and Felder, D.L. (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustacean Issues 12, 817830.Google Scholar
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, 193199.Google Scholar
Stachowicz, J.J. and Hay, M.E. (1996) Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105, 377387.Google Scholar
Stachowicz, J.J. and Hay, M.E. (1999) Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense. Ecology 80, 20852101.Google Scholar
Sturmbauer, C., Levinton, J.S. and Christy, J. (1996) Molecular phylogeny analysis of fiddler crabs: test of the hypothesis of increasing behavioral complexity in evolution. Proceedings of the National Academy of Sciences 93, 1085510857.Google Scholar
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and other methods), version 4.010b. Sunderland, MA: Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Wagner, H.P. (1990) The genera Mithrax Latreille, 1818 and Mithraculus White, 1847 (Crustacea: Brachyura: Majidae) in the western Atlantic Ocean. Zoologische Verhandelingen 264, 165.Google Scholar
White, A. (1847) List of the specimens of Crustacea in the collection of the British Museum. London: British Museum.Google Scholar
Williams, A.B. (1984) Shrimps, lobsters and crabs of the Atlantic coast of the eastern United States, Maine to Florida. Washington: Smithsonian Institution Press.Google Scholar
Williams, S.T., Knowlton, N., Weigt, L.A. and Jara, J.A. (2001) Evidence for three major clades within the snapping shrimp genus Alpheus inferred from nuclear and mitochondrial gene sequence data. Molecular Phylogenetics and Evolution 20, 375389.Google Scholar