Abstract
The tropical Indo-West Pacific is the biogeographic region with the highest diversity of marine shallow water species, with its centre in the Indo-Malay Archipelago. However, due to its high endemism, the Red Sea is also considered as an important centre of evolution. Currently, not much is known about exchange among the Red Sea, Indian Ocean and West Pacific, as well as connectivity within the Indo-Malay Archipelago, even though such information is important to illuminate ecological and evolutionary processes that shape marine biodiversity in these regions. In addition, the inference of connectivity among populations is important for conservation. This study aims to test the hypothesis that the Indo-Malay Archipelago and the Red Sea are important centres of evolution by studying the genetic population structure of the giant clam Tridacna maxima. This study is based on a 484-bp fragment of the cytochrome c oxidase I gene from 211 individuals collected at 14 localities in the Indo-West Pacific to infer lineage diversification and gene flow as a measure for connectivity. The analysis showed a significant genetic differentiation among sample sites in the Indo-West Pacific (Φst = 0.74, P < 0.001) and across the Indo-Malay Archipelago (Φst = 0.72, P < 0.001), indicating restricted gene flow. Hierarchical AMOVA revealed the highest fixation index (Φct = 0.8, P < 0.001) when sample sites were assigned to the following regions: (1) Red Sea, (2) Indian Ocean and Java Sea, (3) Indonesian throughflow and seas in the East of Sulawesi, and (4) Western Pacific. Geological history as well as oceanography are important factors that shape the genetic structure of T. maxima in the Indo-Malay Archipelago and Red Sea. The observed deep evolutionary lineages might include cryptic species and this result supports the notion that the Indo-Malay Archipelago and the Red Sea are important centres of evolution.
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Alvarado Bremer JR, Stequert B, Robertson NW, Ely B (1998) Genetic evidence for inter-oceanic subdivision of bigeye tuna (Thunnus obesus Lowe) populations. Mar Biol 132:547–557
Arnaud S, Bonhomme F, Borsa P (1999) Mitochondrial DNA analysis of the genetic relationships among populations of scads mackerel (Decapterus macarellus, D. macrosoma, and D. russelli) in South-East Asia. Mar Biol 135:699–707
Ashworth JS, Ormond RFG, Sturrock HT (2004) Effects of reef-top gathering and fishing on invertebrate abundance across take and no-take zones. J Exp Mar Biol Ecol 303:221–242
Ayala FJ, Hedgecock D, Zumwalt GS, Valentine JW (1973) Genetic variation in Tridacna maxima, an ecological analog of some unsuccessful evolutionary lineages. Evolution 27:177–191
Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport:patterns, causes and consequences. Mol Ecol 11:659–674
Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods:origins and timing of regional lineage diversification in the coral triangle. Evolution 60:1825–1839
Benzie JAH (1999) Major genetic differences between crown-of-thorns starfish (Acanthaster planci) populations in the Indian and Pacific Oceans. Evolution 53:1782–1795
Benzie JAH, Williams ST (1992a) Genetic structure of giant clam (Tridacna maxima) populations from reefs in the Western Coral Sea. Coral Reefs 11:135–141
Benzie JAH, Williams ST (1992b) No genetic differentiation of giant clam (Tridacna gigas) populations in the Great Barrier Reef, Australia. Mar Biol 112:1–5
Benzie JAH, Williams ST (1995) Gene flow among giant clam (Tridacna gigas) populations in Pacific does not parallel ocean circulation. Mar Biol 123:781–787
Benzie JAH, Williams ST (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
Benzie JAH, Ballment E, Forbes AT, Demetriades NT, Sugama K, Haryanti Moria S (2002) Mitochondrial DNA variation in Indo-Pacific populations of the tiger prawn, Peneus monodon. Mol Ecol 11:2553–2569
Borsa P (2003) Genetic structure of round scad mackerel Decapterus macrosoma (Carangidae) in the Indo-Malay Archipelago. Mar Biol 142:575–581
Briggs JC (1999) Coincident biogeographic patterns: Indo-West Pacific Ocean. Evolution 53:326–335
Campbell CA, Valentine JW, Ayala FJ (1975) High genetic variability in a population of Tridacna maxima from the Great Barrier Reef. Mar Biol 33:341–345
Chenoweth SF, Hughes JM (2003) Oceanic interchange and nonequilibrium population structure in the estuarine dependent Indo-Pacific tasselfish, Polynemus sheridani. Mol Ecol 12:2387–2397
Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) When oceans meet:a teleost shows secondary integration at an Indian-Pacific interface. Proc R Soc Lond B Biol Sci 265:415–420
Chow S, Okamoto H, Uozumi Y, Takeuchi Y, Takeyama H (1997) Genetic stock structure of the swordfish (Xiphias gladius) inferred by PCR-RFLP analysis of the mitochondrial DNA control region. Mar Biol 127:359–367
Chow S, Okamoto H, Miyabe N, Hiramatsu K, Barut N (2000) Genetic divergence between Atlantic and Indo-Pacific stocks of bigeye tuna (Thunnus obesus) and admixture around South Africa. Mol Ecol 9:221–227
Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626
Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415
De Boer TS, Subia MD, Ambariyanto Erdmann MV, Kovitvongsa K, Barber PH (2008) Phylogeography and limited genetic connectivity in the endangered giant boring clam, Tridacna crocea, across the Coral Triangle. Conserv Biol 22:1255–1266
Duda TF, Palumbi SR (1999) Population structure of the black tiger prawn, Penaeus monodon, among western Indian Ocean and western Pacific populations. Mar Biol 134:705–710
Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328
Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and coral biodiversity in indonesia:Effects of land-based pollution, destructive fishing practices and changes over time. Mar Pollut Bull 36:617–630
Erdmann M (1995) An ABC guide to coral reef fisheries in southwest Sulawesi, Indonesia. Naga, ICLARM Quarterly 18(2):4–6
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes:application to human mitochondrial DNA restriction data. Genetics 131:479–491
Fauvelot C, Bernardi G, Planes S (2003) Reduction in the mitochondrial DNA diversity of coral reef fish provides evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583
Fox HE, Mous PS, Pet JS, Muljadi AH, Caldwell RL (2005) Experimental assessment of coral reef rehabilitation following blast fishing. Conserv Biol 19:98–107
Fratini S, Vannini M (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda:Portunidae) within the Indian Ocean. J Exp Mar Biol Ecol 272:103–116
Froukh T, Kochzius M (2007) Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea. Mol Ecol 16:1359–1367
Froukh T, Kochzius M (2008) Species boundaries and evolutionary lineages in the blue green damselfishes Chromis viridis and C. atripectoralis (Pomacentridae). J Fish Biol 72:451–457
Fu FX (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Godfrey JS (1996) The effect of the Indonesian throughflow on ocean circulation and heat exchange with the atmosphere:A review. J Geophys Res 101:12217–12238
Godfrey JS, Masumoto (1999) Diagnosing the mean strength of the Indonesian Throughflow in an ocean general circulation model. J Geophys Res 104:7889–7895
Gordon AL (2005) Oceanography of the Indonesian seas and their throughflow. Oceanography 18:14–27
Gordon AL, Fine RA (1996) Pathways of water between the Pacific and Indian oceans in the Indonesian seas. Nature 379:146–149
Goren M, Dor M (1994) An updated checklist of the fishes of the Red Sea–CLOFRES II. Israel Academy of Sciences and Humanities, Jerusalem
Hall TA (1999) BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98
Hassan M, Harmelin-Vivien M, Bonhomme F (2003) Lessepsian invasion without bottleneck:examples of two rabbitfish species (Siganus rivulatus and Siganus luridus). J Exp Mar Biol Ecol 291:219–232
Hendiarti N, Siegel H, Ohde T (2004) Investigation of different coastal processes in Indonesian waters using SeaWiFS data. Deep-Sea Res Pt II 51:85–97
Hoeksema BW (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the coral triangle. In: Renema W (ed) Biogeography, time and place: distributions, barriers and islands, Top Geobiol 29: 117–178
Hopley D, Suharsono (2000) The Status of coral reefs in eastern Indonesia. Global Coral Reef Monitoring Network (GCRMN)
Imron Jeffrey B, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecol 16:289–304
Ishikura M, Adachi K, Maruyama T (1999) Zooxanthellae release glucose in the tissue of a giant clam, Tridacna crocea. Mar Biol 133:665–673
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance web service. BMC Genet 6:13
Jokiel P, Martinelli FJ (1992) The vortex model of coral reef biogeography. J Biogeogr 19:449–458
Juinio-Meñez MA, Magsino RM, Ravago-Gotanco R, Yu ET (2003) Genetic structure of Linckia laevigata and Tridacna crocea populations in the Palawan shelf and shoal reefs. Mar Biol 142:717–726
Kittiwattanawong K (1997) Genetic structure of giant clam, Tridacna maxima in the Andaman Sea, Thailand. Spec Publ Phuket Mar Biol Cent 17:109–114
Kittiwattanawong K, Nugranad J, Srisawat T (2001) High genetic divergence of Tridacna squamosa living at the west and east coasts of Thailand. Spec Publ Phuket Mar Biol Cent 25:343–347
Klausewitz W (1989) Evolutionary history and zoogeography of the Red Sea ichthyofauna. Fauna of Saudi Arabia 10:310–337
Knittweis L, Krämer WE, Timm J, Kochzius M (2009) Genetic structure of Heliofungia actiniformis (Scleractinia:Fungiidae) populations in the Indo-Malay Archipelago:implications for live coral trade management efforts. Conserv Genet 10:241–249
Kochzius M, Blohm D (2005) Genetic population structure of the lionfish Pterois miles (Scorpaenidae, Pteroinae) in the Gulf of Aqaba and northern Red Sea. Gene 347:295–301
Kochzius M, Nuryanto A (2008) Strong genetic population structure in the boring giant clam Tridacna crocea across the Indo-Malay Archipelago:implications related to evolutionary processes and connectivity. Mol Ecol 17:3775–3787
Kochzius M, Söller R, Khalaf MA, Blohm D (2003) Molecular phylogeny of the lionfish genera Dendrochirus and Pterois (Scorpaenidae, Pteroinae) based on mitochondrial DNA sequences. Mol Phylogenet Evol 28:396–403
Laurent V, Planes S, Salvat B (2002) High variability of genetic pattern in giant clam (Tridacna maxima) populations within French Polynesia. Biol J Linn Soc 77:221–231
Leggat W, Buck BH, Grice A, Yellowlees D (2003) The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant Cell Environ 26:1951–1961
Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas:global phylogeography of the sea urchin Diadema. Evolution 55:955–975
Lourie SA, Green DM, Vincent ACJ (2005) Dispersal, habitat differences, and comparative phylogeography of Southeast Asian seahorses (Syngnathidae:Hippocampus). Mol Ecol 14:1073–1094
Lucas JS (1988) Giant clams: description, distribution and life history. In: Copland JW, Lucas JS (eds) Giant clams in Asia and the Pacific. Australian Centre for International Agricultural Research, Canberra, pp 21–32
Lucas JS (1994) The biology, exploitation and mariculture of giant clams (Tridacnidae). Rev Fish Sci 2:181–223
Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229
Macaranas JM, Ablan CA, Pante MJR, Benzie JAH, Williams STH (1992) Genetic structure of giant clam (Tridacna derasa) populations from reefs in the Indo-Pacific. Mar Biol 113:231–238
Maier E, Tollrian R, Rinkevich B, Nürnberger B (2005) Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Mar Biol 147:1109–1120
McManus JW (1985) Marine speciation, tectonics and sea-level changes in Southeast Asia. Proc 5th Int Coral Reef Symp 4:133–138
Mous PJ, Pet JS, Arifin Z, Djohani R, Erdmann MV, Halim A, Knight H, Pet-Soede L, Wiadnya G (2005) Policy needs to improve marine capture fisheries management and to define a role for marine protected areas in Indonesia. Fish Manag Ecol 12:259–268
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nei M, Jin L (1989) Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol 6:290–300
Nelson JS, Hoddell RJ, Chou LM, Chan WK, Phang VPE (2000) Phylogeographic structure of false clownfish, Amphiprion ocellaris, explained by sea level changes on the Sunda shelf. Mar Biol 137:727–736
Ovenden JR, Salini JS, O’Connor, Street R (2004) Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei, Perciformes, Lutjanidae) from the East Indies triangle. Mol Ecol 13:1991–1999
Palumbi SR (2001) The ecology of marine protected areas. In: Bertness MD, Gaines SM, Hixon ME (eds) Marine Community Ecology. Sinauer Associates, Sunderland, pp 509–530
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
Pasaribu BP (1988) Status of giant clams in Indonesia. In: Copland JW, Lucas JS (eds) Giant clams in Asia and the Pacific. Australian Centre for International Agricultural Research, Canberra, pp 44–46
Perrin C, Borsa P (2001) Mitochondrial DNA analysis of the geographic structure of Indian scad mackerel in the Indo-Malay Archipelago. J Fish Biol 59:1421–1426
Pet J (1997) Destructive fishing methods in and around Komodo National Park. SPC Live Reef Fish Information Bulletin 2:20–24
Posada D, Crandall KA (1998) Modeltest:testing the model of DNA substitution. Bioinformatics 14:817–818
Ravago-Gotanco RG, Magsino RM, Juinio-Menez MA (2007) Influence of the North Equatorial Current on the population genetic structure of Tridacna crocea (Mollusca:Tridacnidae) along the eastern Philippine seaboard. Mar Ecol Prog Ser 336:161–168
Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006
Richter C, Roa-Quiaoit H, Jantzen C, Al-Zibdah M, Kochzius M (2008) Collapse of a new living species of giant clam in the Red Sea. Curr Biol 18:1349–1354
Ridgway T, Sampayo EM (2005) Population genetic status of the Western Indian Ocean:what do we know? Western Indian Ocean J Mar Sci 4:1–9
Risk MJ, Erdmann MV (2000) Isotopic composition of Nitrogen in stomatopod (Crustacea) tissues as an indicator of human sewage impacts on Indonesian coral reefs. Mar Pollut Bull 40:50–58
Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284
Rogers AR (1995) Genetic evidence for Pleistocene population expansion. Evolution 49:608–615
Rogers AL, Harpending H (1992) Population growth makes in the distribution of pairwise genetics differences. Mol Biol Evol 9:552–569
Rohfritsch A, Borsa P (2005) Genetic structure of Indian scad mackerel Decapterus russelli:Pleistocene vicariance and secondary contact in the Central Indo-West Pacific Seas. Heredity 95:315–326
Schneider S, Roessli D, Excoffier L (2000) Arlequin, version 2.000. University of Geneva, Geneva
Shefer S, Abelson A, Mokady O, Geffen E (2004) Red to Mediterranean Sea bioinvasion:natural drift through the Suez Canal, or anthropogenic transport? Mol Ecol 12:2333–2343
Siddall M, Smeed DA, Matthiesen S, Rohling EJ (2002) Modelling the seasonal cycle of the exchange flow in Bab el Mandab (Red Sea). Deep-Sea Res Pt I 49:1551–1569
Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. UNEP World Conservation Monitoring Centre, University of California Press, Berkeley
Sugama K, Haryanti, Benzie JAH, Ballment E (2002) Genetic variation and population structure of the giant tiger prawn, Penaeus monodon, in Indonesia. Aquaculture 205:37–48
Susanto RD, Gordon AL (2005) Velocity and transport of the Makassar Strait throughflow. J Geophysl Res 110:C01005
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Thompson JG, Higgins DG, Gibson TJ (1994) CLUSTAL W:improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Timm J, Kochzius M (2008) Geological history and oceanography of the Indo-Malay Archipelago shape the genetic population structure in the False Clown Anemonefish (Amphiprion ocellaris). Mol Ecol 17:3999–4014
Timm J, Figiel M, Kochzius M (2008) Contrasting patterns in species boundaries and evolution of anemonefishes (Amphiprioninae, Pomacentridae) in the centre of marine biodiversity. Mol Phylogenet Evol 49:268–276
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science and CRR Qld Pty Ltd
Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia:shorelines, river systems and time duration. J Biogeogr 27:1153–1167
Wabnitz C, Taylor M, Green E, Razak T (2003) From ocean to aquarium. UNEP-WCMC, Cambridge, UK
Walsh PS, Metzger DA, Higushi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513
Wells S (1997) Giant clams:status, trade and mariculture, and the role of CITES management. IUCN, Gland, Switzerland and Cambridge, UK
Wilkinson C (2002) Status of coral reefs of the world:2002. Australian Institute of Marine Science
Williams ST, Benzie JAH (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
Woodland DJ (1983) Zoogeography of the Siganidae (Pisces): an interpretation of distribution and richness pattern. Bull Mar Sci 33:713–717
Wörheide G, Epp LS, Macis L (2008) Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae):Founder effects, vicariance, or both? BMC Evol Biol 8:24
Wyrtki K (1961) Physical oceanography of the Southeast Asian waters. University of California, La Jolla, USA
You E-M, Chiu T-S, Liu K-F, Tassanakajon A, Klinbunga S, Triwitayakorn K, de la Peña LD, Li Y, Yu H-T (2008) Microsatellite and mitochondrial haplotype diversity reveal population differentiation in the tiger shrimp (Peneus monodon) in the Indo-Pacific region. Anim Genet [doi:10.1111/j.1365-2052.2008.01724.x]
Yu ET, Juinio-Meñez MA, Monje VD (2000) Sequence variation in the ribosomal DNA internal transcribed spacer of Tridacna crocea. Mar Biotechnol 2:511–516
Acknowledgement
We would like to thank the institutions and individuals that have made our study possible: German Federal Ministry of Education and Research (BMBF, Grant no. 03F0390B), which funded the project ‘Molecular Genetics as a Tool for the Management of Marine Ornamentals in Sulawesi (Indonesia)’ in the framework of the joint German-Indonesian project SPICE (Science for the Protection of Indonesian Coastal Marine Ecosystems); German Academic Exchange Service (DAAD) for supporting A. Nuryanto; Centre for Tropical Marine Ecology (Bremen, Germany) for project co-ordinated, especially C. Richter; colleagues from the University of Bremen, especially J. Timm for help during field work; colleagues from Universitas Hasanuddin (Makassar, Indonesia) for logistical support in Spermonde, especially J. Jompa; anonymous reviewers for constructive comments. The SPICE project is conducted and permitted under the governmental agreement between the German Federal Ministry of Education and Research (BMBF) and the Indonesian Ministry for Research and Technology (RISTEK), Indonesian Institute of Sciences (LIPI), Indonesian Ministry of Maritime Affairs and Fisheries (DKP), and Agency for the Assessment and Application of Technology (BPPT). This work was carried out in co-operation with Hassanuddin University (UNHAS, Makassar, Indonesia), Agricultural University Bogor (IPB, Bogor, Indonesia), and Jenderal Soedirman University (Purwokerto, Indonesia).
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Nuryanto, A., Kochzius, M. Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima . Coral Reefs 28, 607–619 (2009). https://doi.org/10.1007/s00338-009-0483-y
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DOI: https://doi.org/10.1007/s00338-009-0483-y