Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-27T05:12:55.670Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeography of the planktonic shrimp Lucifer hanseni Nobili 1905 in the Indo-Malayan Archipelago

Published online by Cambridge University Press:  24 February 2016

Mary Mar Noblezada ,
Hiroomi Miyamoto ,
Wilfredo L. Campos ,
Fatimah MD. Yusoff  and
Shuhei Nishida
Mary Mar Noblezada*
Affiliation:
Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa 277-8564, Japan The Marine Science Institute, University of the Philippines Diliman, Velasquez St., 1101 Quezon City, Philippines OceanBio Laboratory, Division of Biological Sciences, College of Arts and Sciences, The University of Philippines Visayas, 5023 Miagao, Iloilo, Philippines
Hiroomi Miyamoto
Affiliation:
Tohuku National Fisheries Research Institute, Fisheries Research Agency, 3-27-5 Shinhama, Shiogama 985-0001, Japan
Wilfredo L. Campos
Affiliation:
OceanBio Laboratory, Division of Biological Sciences, College of Arts and Sciences, The University of Philippines Visayas, 5023 Miagao, Iloilo, Philippines
Fatimah MD. Yusoff
Affiliation:
Department of Aquaculture, Faculty of Agriculture, Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia
Shuhei Nishida
Affiliation:
Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa 277-8564, Japan
*
Correspondence should be addressed to:M.M. Noblezada, Atmosphere and Ocean Research Institute, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa 277-8564, Japan email: mmpnoblezada@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Using partial sequences of two mitochondrial genes, cytochrome c oxidase subunit I (COI) and 12S ribosomal RNA (12S rRNA), and one nuclear gene, 28S ribosomal RNA (28S rRNA), we investigated population genetics of the holoplanktonic shrimp Lucifer hanseni Nobili, 1905 in the Indo-Malayan Archipelago (IMA), encompassing Andaman Sea, Malacca Strait, Gulf of Thailand, Borneo Island, Philippines (hereafter collectively referred to as the Thailand-Malaysia-Philippine area: TMP), Celebes Sea (CS), and the waters near islands in the Western Pacific (WP) including Palau, Papua New Guinea and Solomon Islands. The samples from the TMP showed the highest number of haplotypes. Significant phylogeographic structure was found in the L. hanseni populations (ΦST = 0.832 for COI, 0.159 for 12S rRNA, 0.783 for 28S rRNA). The total number of haplotypes was 46 in COI, 28 in 12S rRNA and 23 in 28S rRNA. The haplotype network analyses revealed two major clades for COI (subgroups: TMP + CS, WP) and for 12S rRNA and 28S rRNA (TMP, CS + WP). The CS and WP populations appeared isolated from the TMP populations. The samples from the CS showed low genetic diversity compared with the other samples at both haplotype and nucleotide levels, suggesting that the population CS experienced bottleneck events. This is the first demonstration of significant genetic structure of a holoplanktonic metazoan in IMA, which is suggested to be synergistically influenced by historical events (vicariance) and contemporary oceanographic circulations and corroborates the results of previous studies on other benthic/demersal animals with mero-planktonic phases.

Keywords

Lucifer hanseniIndo-Malayan Archipelagophylogeography
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 1 , February 2017 , pp. 129 - 140
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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

Bandelt, H.J., Forster, P. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.Google Scholar
Barber, P.H., Moosa, M.K. and Palumbi, S.R. (2002a) Rapid recovery of genetic diversity of stomatopod populations on Krakatau: temporal and spatial scales of marine larval dispersal. Proceedings of the Royal Society of London Series B – Biological Sciences 269, 1591–1597.Google Scholar
Barber, P.H., Palumbi, S.R., Erdmann, M.V. and Moosa, M.K. (2000) Biogeography: a marine Wallace's line? Nature 406, 692–693.CrossRefGoogle ScholarPubMed
Barber, P.H., Palumbi, S.R., Erdmann, M.V. and Moosa, M.K. (2002b) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Molecular Ecology 11, 659–674.CrossRefGoogle ScholarPubMed
Benzie, J.A. (1998) Genetic structure of marine organisms and SE Asian biogeography. In Hall, R. and Holloway, J.D. (eds) Biogeography and geological evolution of South East Asia. Leiden: Backhuys Publishers, pp. 197–210.Google Scholar
Benzie, J.A. (1999) Major genetic differences between crown-of-thorns starfish (Acanthaster planci) populations in the Indian and Pacific Oceans. Evolution 53, 1782–1795.Google Scholar
Benzie, J.A. and Williams, S.T. (1997) Genetic structure of giant clam (Tridacna maxima) populations in the West Pacific is not consistent with dispersal by present-day ocean currents. Evolution 51, 768–783.Google Scholar
Blanco-Bercial, L., Alvarez-Marquez, F. and Bucklin, A. (2011) Comparative phylogeography and connectivity of sibling species of the marine copepod Clausocalanus (Calanoida). Journal of Experimental Marine Biology and Ecology 404, 108–115.Google Scholar
Borsa, P. (2003) Genetic structure of round scad mackerel Decapterus macrosoma (Carangidae) in the Indo-Malay archipelago. Marine Biology 142, 575–581.Google Scholar
Brito, P.H. and Edwards, S.V. (2009) Multilocus phylogeography and phylogenetics using sequence-based markers. Genetics 135, 439–455.Google Scholar
Carpenter, K.E. (1998) An introduction to the oceanography, geology, biogeography, and fisheries of the tropical and subtropical western and central Pacific. In Carpenter, K.E. and Niem, V.H. (eds) The living marine resources of the western central Pacific. FAO species identification guide for fishery purposes. Rome: FAO, pp. 1–17.Google Scholar
Carpenter, K.E. and Springer, V.G. (2005) The center of marine shore fish biodiversity: the Philippine Islands. Environmental Biology of Fishes 72, 467–480.CrossRefGoogle Scholar
Carpenter, K.E., Barber, P.H., Crandall, E.D., Ablan-Lagman, M.C.A., Ambariyanto, Mahardika N.G., Manjaji-Matsumoto, M.B., Junio-Meñez, 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 2011, Article 396982. doi: 10.1155/2011/396982. Google Scholar
Chen, G. and Hare, M.P. (2011) Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast. Molecular Ecology 20, 2425–2441.Google Scholar
Coyne, J.A. and Orr, H.A. (2004) Speciation. Sunderland, MA: Sinauer Associates Inc. Google Scholar
Crandall, E.D., Frey, M.A., Grosberg, R.K. and Barber, P.H. (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Molecular Ecology 17, 611–626.Google Scholar
Dakin, J.W. and Colefax, N.A. (1940) The plankton of the Australian coastal waters off New South Wales. Publications of the University of Sydney, Department of Zoology, Monograph 1, 215 pp.Google Scholar
Dawson, M.N. and Jacobs, D.K. (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin 200, 92–96.Google Scholar
DeBoer, T.S., Subia, M.D., Ambariyanto, Erdmann M.V., Kovitvongsa, K. and Barber, P.H. (2008) Phylogeography and limited genetic connectivity in the endangered boring giant clam across the Coral Triangle. Conservation Biology 22, 1255–1266.Google Scholar
De Grave, S., Einav, R. and Galil, B.S. (2012) Recent records of the Indo-Pacific species, Lucifer hanseni Nobili, 1905 (Crustacea; Decapoda; Luciferidae) from the Mediterranean coast of Israel. Bio Invasions Record 1, 105–108.Google Scholar
Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierrer, T. and Wilson, A. (2010) Geneious v. 5.3. http://www.geneious.com/ Google Scholar
Excoffier, L., Laval, G. and Schneider, S. (2007) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Farfante, I.P. and Kensley, B. (1997) Penaeoid and sergestoid shrimps and prawns of the world: keys and diagnoses for the families and genera. Memoires du Museum National d'Histoire Naturelle, Paris 175, 1–233.Google Scholar
Fleminger, A. (1986) The Pleistocene equatorial barrier between the Indian and Pacific Oceans and a likely cause for Wallace's line. In Pierrot-Bults, A.C., van der Spoel, S., Zarhuranec, B.J. and Johnson, R.K. (eds) Pelagic biogeography. UNESCO Technical Papers in Marine Science Volume 49. Paris: United Nations Educational Scientific and Cultural Organization, pp. 84–97.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Goetze, E. (2011) Population differentiation in the open sea: insights from the pelagic copepod Pleuromamma xiphias . Integrative Comparative Biology 51, 580–597.Google Scholar
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.CrossRefGoogle Scholar
Goswami, S.C. and Shrivastava, Y. (1996) Zooplankton standing stock, community structure and diversity in the Northern Arabian Sea. Proceedings on the Second Workshop on Scientific Research. FORV Sagar, Sampada, pp. 127–137.Google Scholar
Grabe, S.A. and Lee, D.C. (1992) Macrozooplankton studies in Kuwait Bay (Arabian Gulf). II. Distribution and composition of planktonic penaeidae. Journal of Plankton Research 14, 1673–1686.Google Scholar
Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. System Biology 52, 696–704.Google Scholar
Gurney, R. (1924) Zoological results of the Cambridge expedition to the Suez Canal, XV. Report on the larvae of the Crustacea, Decapoda. Transactions of the Zoological Society of London 22, 246–251.Google Scholar
Hanebuth, T., Stattegger, K. and Grootes, P.M. (2000) Rapid flooding of the Sunda Shelf: a late glacial sea-level record. Science 288, 1033–1035.Google Scholar
Hall, R. (2002) Cenozoic gelogical and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Science 20, 353–431.CrossRefGoogle Scholar
Hare, M.P. (2001) Prospects for nuclear gene phylogeography. Trends in Ecology and Evolution 16, 700–706.Google Scholar
Hashizume, K. and Omori, M. (1998) Distribution of warm epiplanktonic shrimp of the genus Lucifer (Decapoda: Dendrobranchiata: Sergestinae) in the northwestern Pacific Ocean with special reference to their adaptive features. IOC Workshop Report 142, 156–162.Google Scholar
Herbert, P.D.N., Ratnasingham, S. and deWaard, R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. B (Suppl.) , S96–S99. doi: 10.1098/rsbl.2003.0025.Google Scholar
Huang, M. and Fang, J. (1987) Distribution of Lucifer and its relation to fishery in Taiwan Strait and its adjacent areas. Journal of Oceanography of Taiwan Strait 6, 107–113. [In Chinese]Google Scholar
Hudson, R.R. and Coyne, J.A. (2002) Mathematical consequences of the genealogical species concept. Evolution 56, 1557–1565.Google ScholarPubMed
Kochzius, M., Seidel, C., Hauschild, J., Kirchhoff, S., Mester, P., Meyer-Wachsmuth, I., Nuryanto, A. and Timm, J. (2009) Genetic population structures of the blue starfish Linckia laevigata and its gastropod ectoparasite Thyca crystallina . Marine Ecology Progress Series 396, 211–219.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Lin, J.H., Chen, R.X., Lin, M. and Dai, Y.Y. (1998) Distribution of zooplankton in Sansha Bay and its comparison with that in Xinghua Bay and Dongshan Bay. Journal of Oceanography of Taiwan Strait 7, 426–432.Google Scholar
Lind, C.E., Brad, E.S., Elphinstone, M.S., Taylor, J.J.U. and Jerry, D.R. (2012) Phylogeography of a pearl oyster (Pinctada maxima) across the Indo-Australian Archipelago: evidence of strong regional structure and population expansions but no phylogenetic breaks. Biological Journal of the Linnean Society 107, 632–646.Google Scholar
Machida, R.J. and Knowlton, N. (2010) PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PLoS ONE 7, e46180. doi: 10.1371/journal.pone0046180. Google Scholar
Machida, R.J., Miya, M.U., Nishida, M. and Nishida, S. (2012) Complete mitochondrial DNA sequence of Tigriopus japonicas (Crustacea: Copepoda). Marine Biotechnology 4, 406–417.Google Scholar
McManus, J.W. (1985) Marine speciation, tectonics and sea level changes in Southeast Asia. Proceedings of the Fifth International Coral Reef Congress May 27–June 1, 1985, Tahiti. Antenne Museum-EPHE. Tahiti, pp. 133–138.Google Scholar
McMillan, W.O. and Palumbi, S.R. (1995) Concordant evolutionary patterns among Indo-West Pacific butterfly fishes. Proceedings of the Royal Society of London. Series B, Biological Sciences 260, 229–236.Google Scholar
Miyamoto, H.R., Machida, R.J. and Nishida, S. (2010) Genetic diversity and cryptic speciation of the deep chaetognath Caecosagitta macrocephala (Fowler, 1904). Deep Sea Research Part II 57, 2211–2219.Google Scholar
Morey, S.L., Shriver, J.F. and O'Brien, J.J. (1999) The effects of Halmahera on the Indonesian throughflow. Journal of Geophysical Research Oceans 104, 23281–23296.Google Scholar
Naomi, T.S., Geetha, A., George, R.M. and Jasmine, S. (2006) Monograph on the planktonic shrimps of the genus Lucifer (Family Luciferidae) from the Indian EEZ. Central Marine Fisheries Research Institute Bulletin 49, 1–54.Google Scholar
Nobili, G. (1905) Faune carcinologique de la Mar Rouge. Decapodes et Stomatopodes. Annales Zoologici Societatis Zoologicae – Botanicae Fennicae ‘Vanamo’ 9, 1–347. Paris: Masson et Cie.Google Scholar
Norris, R.D. (2000) Pelagic species diversity, biogeography, and evolution. Paleobiology 26S, 236–258.Google Scholar
Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.Google Scholar
Omori, M. (1977) Distribution of warm water epiplanktonic shrimps of the genera Lucifer and Acetes (Macrura, Penaeidea, Segestidae). Proceedings of the Symposium on Warm Water Zooplankton, 1977 October 14–19; Goa, India. Goa: National Institute of Oceanography, pp. 1–12.Google Scholar
Palumbi, S.R. (1992) Marine speciation on a small planet. Trends in Ecology and Evolution 7, 114–118.CrossRefGoogle ScholarPubMed
Peijnenburg, K.T.C.A., Breeuwer, J.A.J., Pierrot-Bults, A.C. and Menken, S.B.J. (2004) Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European seas. Evolution 58, 1472–1487.Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Tan, Y.H., Huang, L.M., Chen, Q.C. and Huang, X.P. (2004) Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China. Continental Shelf Research 24, 1949–1968.Google Scholar
Thompson, J.D., Gibdon, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Tittensor, D.P., Mora, C., Jetz, W., Lotze, H.K., Richard, D., Berghe, E.V. and Worm, B. (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101.CrossRefGoogle ScholarPubMed
Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 27, 1153–1167.CrossRefGoogle Scholar
Williams, S.T. and Benzie, J.A.H. (1997) Indo-West Pacific patterns of genetic differentiation in the high dispersal starfish Linckia laevigata . Molecular Ecology 6, 559–573.Google Scholar
Williams, S.T. and Benzie, J.A.H. (1998) Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mtDNA, and allozyme data. Evolution 52, 87–99.Google Scholar
Woodruff, D.S. (2010) Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today's patterns and the future of the remaining refugial-phase biodiversity. Biodiversity and Conservation 19, 919–941.Google Scholar
Wörheide, G., Sole-Cava, M.A. and Hooper, J.N.A. (2005) Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks. Integrative and Comparative Biology 45, 377–385.CrossRefGoogle ScholarPubMed
Zhou, X.D. and Xu, Z.L. (2009) Ecological characteristics of the pelagic decapods in the Changjiang Estuary. Journal of Fisheries China 33, 30–36.Google Scholar