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Patiriella pseudoexigua (Asteroidea: Asterinidae): a cryptic species complex revealed by molecular and embryological analyses

Published online by Cambridge University Press:  19 September 2003

Michael W. Hart ,
Maria Byrne  and
Sheri L. Johnson
Michael W. Hart*
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada
Maria Byrne
Affiliation:
Department of Anatomy and Histology, F-13, University of Sydney, Sydney, New South Wales 2006, Australia
Sheri L. Johnson
Affiliation:
Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada Darling Marine Center, University of Maine, Walpole, ME 04573, USA
*
∫Corresponding author, e-mail: michael.hart@dal.ca
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Abstract

Cryptic lineages were identified within a morphologically uniform group of sea stars distributed from Australia to Japan. Among eight populations, all of which have been referred to Patiriella pseudoexigua, we found seven unique mitochondrial DNA sequences clustered into four distinct lineages. These four lineages formed a monophyletic group in which sister clades were separated by small genetic distances but could be differentiated from each other on the basis of reproductive differences. The four lineages thus appear to be separate but very closely related species. Examination of reproduction in several Queensland populations revealed that one population (Statue Bay) consisted of hermaphroditic intragonadal brooders with live-born offspring while other populations (Townsville, Bowen, Airlie Beach) consisted of dioecious free-spawners with a planktonic larva. The brooded larvae from central Queensland populations closely resembled brooded embryos and larvae of a Japanese lineage, while the planktonic larvae from northern Queensland were similar to the original description of planktonic larvae from a Taiwan population. However, each of the viviparous lineages was more closely related to a lineage with planktonic larval development than the viviparous lineages were to each other. Patiriella pseudoexigua thus comprises at least four species with different reproductive phenotypes in which viviparous brooding appears to have evolved in parallel. Based on previous taxonomic work we propose the following names for these four lineages: the dioecious free-spawner from northern Queensland (including the P. pseudoexigua type locality) is P. pseudoexiguasensu stricto; the viviparous brooder from central Queensland is undescribed and here referred to as Patiriella sp. nov; the dioecious free-spawner from Taiwan is temporarily referred to as Patiriella sp. (a senior name for this species may be P. pentagonus); and the hermaphrodite brooder from Japan should be raised to specific status and referred to by the new combination P. pacifica.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 83 , Issue 5 , October 2003 , pp. 1109 - 1116
Copyright
Copyright © Marine Biological Association of the United Kingdom 2003

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References

Arndt, A. & Smith, M.J., 1998. Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Molecular Ecology, 7, 1053–1064.CrossRefGoogle Scholar
Asakawa, S., Himeno, H., Miura, K. & Watanabe, K., 1995. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics, 140, 1047–1060.Google ScholarPubMed
Baric, S. & Sturmbauer, C., 1999. Ecological parallelism and cryptic species in the genus Ophiothrix derived from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 11, 157–162.Google Scholar
Briggs, J.C., 1974. Marine zoogeography. New York: McGraw-Hill.Google Scholar
Byrne, M. & Anderson, M.J., 1994. Hybridization of sympatric Patiriella species (Echinodermata: Asteroidea) in New South Wales. Evolution, 48, 564–576.Google Scholar
Byrne, M. & Cerra, A., 1996. Evolution of intragonadal develop-ment in the diminutive asterinid sea stars Patiriella vivipara and P. parvivipara with an overview of development in the Asterinidae. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 191, 17–26.Google Scholar
Byrne, M., Cerra, A., Hart, M. & Smith, M., 1999a. Life history diversity and molecular phylogeny in the Australian sea star genus Patiriella. In The other 99%: the conservation and biodiversity of invertebrates (ed. W Ponder and D. Lunney), pp. 188–196. Sydney: Royal Zoological Society of New South Wales.Google Scholar
Byrne, M., Cerra, A. & Villinski, J.T., 1999b. Oogenic strategies in the evolution of development in Patiriella (Echinodermata: Asteroidea). Invertebrate Reproduction and Development, 36, 195–202.Google Scholar
Campbell, A.C. & Rowe, F.E.W., 1995. A new species in the asterinid genus Patiriella (Echinodermata, Asteroidea) from Dhofar, southern Oman: a temperate taxon in a tropical locality. Bulletin of the Natural History Museum of London (Zoology), 63, 129–136.Google Scholar
Chen, B.Y. & Chen, C.-P., 1992. Reproductive cycle, larval devel-opment, juvenile growth and population dynamics of Patiriella pseudoexigua (Echinodermata, Asteroidea) in Taiwan. Marine Biology, 113, 271–280.Google Scholar
Chia, F.-S. & Walker, C.W., 1991. Echinodermata: Asteroidea. In Reproduction of marine invertebrates. Vol. 6. Echinoderms and lophophorates (ed. A.C. Geise et al.), pp. 301–353. Pacific Grove, CA: The Boxwood Press.Google Scholar
Clark, A.M., 1983. Notes on Atlantic and other Asteroidea. 3. The families Ganeriidae and Asterinidae, with description of a new asterinid genus. Bulletin of the British Museum of Natural History (Zoology), 45, 359–380.Google Scholar
Clark, A.M., 1993. An index of names of recent Asteroidea. Part 2. Valvatida. Echinoderm Studies, 4, 187–366.Google Scholar
Clark, A.M. & Downey, M.E., 1992. Starfishes of the Atlantic. London: Chapman & Hall.Google Scholar
Dartnall, A.J., 1971. Australian sea stars of the genus Patiriella (Asteroidea: Asterinidae). Proceedings of the Linnean Society of New South Wales, 96, 39–49.Google Scholar
Dawson, M.N. & Jacobs, D.K., 2001. Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 200, 92–96.Google Scholar
Emson, R.H. & Crump, R.G., 1979. Description of a new species of Asterina (Asteroidea), with an account of its ecology. Journal of the Marine Biological Association of the United Kingdom, 59, 77–94.Google Scholar
Flowers, J.M. & Foltz, D.W., 2001. Reconciling molecular systematics and traditional taxonomy in a species-rich clade of sea stars (Leptasterias subgenus Hexasterias). Marine Biology, 139, 475–483.Google Scholar
Foltz, D.W., 1997. Hybridization frequency is negatively correlated with divergence time of mitochondrial DNA haplotypes in a sea star (Leptasterias spp.) species complex. Evolution, 51, 283–388.Google ScholarPubMed
Hart, M.W., Byrne, M. & Smith, M.J., 1997. Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution, 51, 1848–1861.Google Scholar
Hayashi, R., 1977. A new sea-star of Asterina from Japan, Asterina pseudoexigua pacifica n. ssp. Proceedings of the Japan Society of Systematic Zoology, 13, 88–91.Google Scholar
Higgins, D.G. & Sharp, P.M., 1988. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene, 73, 237–244.Google Scholar
Knowlton, N., 1993. Sibling species in the sea. Annual Reviews of Ecology and Systematics, 24, 189–216.Google Scholar
Knowlton, N., 2000. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia, 420, 73–90.Google Scholar
Komatsu, M., Kano, Y.T. & Oguro, C., 1990. Development of a true ovoviviparous sea star, Asterina pseudoexigua pacifica Hayashi. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 179, 254–263.Google Scholar
Larsen, K., 2001. Morphological and molecular investigation of polymorphism and cryptic species in tanaid crustaceans: implications for tanaid systematics and biodiversity estimates. Zoological Journal of the Linnean Society, 131, 353–379.Google Scholar
Lazoski, C., Sole-Cava, A.M., Boury-Esnault, N., Klautau, M. & Russo, C. A.M., 2001. Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Marine Biology, 139, 421–429.Google Scholar
Marsh, L.M., 1977. Coral reef asteroids of Palau, Caroline Islands. Micronesica, 13, 251–281.Google Scholar
McEdward, L.R., 1992. Morphology and development of a unique type of pelagic larva in the starfish Pteraster tesselatus (Echinodermata: Asteroidea). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 182, 177–187.Google ScholarPubMed
O'Loughlin, P.M., Waters, J.M. & Roy, M.S., 2002. Description of a new species of Patiriella from New Zealand and review of Patiriella regularis (Echinodermata, Asteroidea) based on morphological and molecular data. Journal of the Royal Society of New Zealand, 32, 697–711.Google Scholar
Oppen, M.J.H. van, McDonald, B.J., Willis, B. & Miller, D., 2001. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Molecular Biology and Evolution, 18, 1315–1329.Google Scholar
Palumbi, S.R., 1992. Marine speciation on a small planet. Trends in Ecology and Evolution, 7, 114–118.CrossRefGoogle Scholar
Palumbi, S.R., 1994. Reproductive isolation, genetic divergence, and speciation in the sea. Annual Reviews of Ecology and Systematics, 25, 547–572.Google Scholar
Palumbi, S.R. & Wilson, A.C., 1990. Mitochondrial DNA diversity in the sea urchins Strongylocentrotus purpuratus and Strongylocentrotus droebachiensis. Evolution, 44, 403–415.Google ScholarPubMed
Pape, T., McKillup, S.C. & McKillup, R.V., 2000. Two new species of Sarcophaga (Sarcorohdendorfid) Baranov (diptera: Sarcophagidae), parasitoids of Littoraria filosa (Sowerby) (Gastropoda: Littorinidae). Australian Journal of Entomology, 39, 236–240.Google Scholar
Quattro, J.M., Chase, M.R., Rex, M.A., Greig, T.W. & Etter, R.J., 2001. Extreme mitochondrial DNA divergence within populations of the deep-sea gastropod Frigidoalvania brychia. Marine Biology, 139, 1107–1113.Google Scholar
Rocha-Olivares, A., Fleeger, J.W. & Foltz, D.W., 2001. Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod. Molecular Biology and Evolution, 18, 1088–1102.CrossRefGoogle Scholar
Rowe, F.W.E. & Gates, J., 1995. Echinodermata. In Zoological catalogue of Australia, vol. 33 (ed. A. Wells), pp. 1–510. Melbourne: CSIRO.Google Scholar
Strathmann, R.R. & Eernisse, D.J., 1994. What molecular phylogenies tell us about the evolution of larval form. American Zoologist, 34, 502–512.Google Scholar
Strathmann, R.R., Strathmann, M.F. & Emson, R.H., 1984. Does limited brood capacity link adult size, brooding, and simultaneous hermaphroditism? A test with the starfish Asterinaphylactica. American Naturalist, 123, 796–818.Google Scholar
Swofford, D.L., 2002. PAUP*:phylogeneticanalysisusingparsimony (and other methods), version 4.0b10. Sunderland: Sinauer Associates.Google Scholar
Tarjuelo, I., Posada, D., Crandall, K.A., Pascual, M. & Turon, X., 2001. Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Marine Biology, 139, 455–462.Google Scholar
Williams, S.T., 2000. Species boundaries in the starfish genus Linckia. Marine Biology, 136, 137–148.Google Scholar
Williams, S.T., Knowlton, N., Weigt, L.A. & 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, 375–389.Google Scholar
Wilson, B.R. & Allen, G.R., 1987. Major components and distri-bution of marine fauna. In Fauna of Australia, vol. 1A (ed. G.R. Dyne and D.W. Walton), pp. 43–68. Canberra: Australian Government Printing Service.Google Scholar