Abstract
Many studies, using various marker systems, have been conducted on the genetic population structure of marine organisms to reveal connectivity among locations and dispersal capabilities. Although mitochondrial sequence markers are widely used, their accuracy is controversially discussed in the context of small scale population genetic discrimination. In the present study, the genetic population structure of the False Clown Anemonefish (Amphiprion ocellaris) in the Indo-Malay Archipelago was revealed by screening six microsatellite loci. Results were congruent to previous mitochondrial control region results, with three major genetic breaks within the Indo-Malay Archipelago. Similar to the mitochondrial DNA (mtDNA) analysis, microsatellite data showed a correlation of genetic structure to historical ocean basin separation during Pleistocene sea level low stands, geographic distance, and dominant current patterns. However, microsatellite divergences are not as deep as the mtDNA divergence, suggesting either that admixture of mtDNA lineages is slower than that of nuclear microsatellites, providing a rather historic picture of separation, or the stronger differentiation signal is due to lower effective population sizes presented by mtDNA. As well, the microsatellite analysis did not give a better resolution on the small scale as expected. This study showed that depending on the genetic markers used, different stages of population separation might be illuminated.
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References
Allen GR, Werner TB (2002) Coral reef fish assessment in the “coral triangle” of southeastern Asia. Environ Biol Fish 65:209–214
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
Barrière A, Félix M (2007) Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations. Genetics 176:999–1011
Barrowclough GF, Zink RM (2009) Funds enough, and time: mtDNA, nuDNA and the discovery of divergence. Mol Ecol 18:2934–2936
Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
Bentzen P, Taggart CT, Ruzzante DE, Cook D (1996) Microsatellite polymorphism and the population structure of Atlantic cod (Gadus morhua) in the northwest Atlantic. Can J Fish Aquat Sci 53:2706–2721
Berry OF (2006) Mitochondrial DNA and population size. Science 314:1388
Borsa P (2003) Genetic structure of the round scad mackerel Decapterus macrosoma (Carangidae) in the Indo-Malay archipelago. Mar Biol 142:575–581
Bradbury IR, Snelgrove PVR (2001) Contrasting larval transport in demersal fish and benthic invertebrates: the role of behaviour and advective processes in determining spatial pattern. Can J Fish Aquat Sci 58:811–823
Briggs JC (2000) Centrifugal speciation and centres of origin. J Biogeogr 27:1183–1188
Buston PM, Bogdanowicz AW, Harrison RG (2007) Are clownfish groups composed of close relatives? An analysis of microsatellite DNA variation in Amphiprion percula. Mol Ecol 16:3671–3678
De Innocentiis S, Sola L, Catandella S, Bentzen P (2001) Allozyme and microsatellite loci provide discordant estimates of population differentiation in the endangered dusky grouper (Epinephelus marginatus) within the Mediterranean Sea. Mol Ecol 10:2163–2175
Edwards S, Bensch S (2009) Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Mol Ecol 18:2930–2933
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50
Eyre-Walker A (2006) Size does not matter for mitochondrial DNA. Science 312:537–538
Fautin DG, Allen GR (1994) Anemonenfische und ihre Wirte. Tetra-Verlag, Melle, pp 1–168
Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583
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 Chromis atripectoralis (Pomacentridae). J Fish Biol 72:451–457
García De Leon FJ, Chikhi L, Bonhomme F (1997) Microsatellite polymorphism and population subdivision in natural populations of European sea bass Dicentrarchus labrax (Linnaeus 1758). Mol Ecol 6:51–62
Garza JC, Slatkin M, Freimer NB (1995) Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol Biol Evol 12:594–603
Glaubitz JC (2004) CONVERT: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310
Goudet J (1995) Fstat version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486
Györffy B, Kocsis I, Vásárhelyi B (2004) Biallelic genotype distributions in papers published in gut between 1998 and 2003: altered conclusions after recalculating the Hardy-Weinberg equilibrium. Int J Gastroenterol Hepatol 53:614–616
Hall R (1996) Reconstructing cenozoic SE Asia. In: Hall R, Blundell D (eds) Tectonic evolution of southeast Asia. Geological Society of London Special Publication No. 106, pp. 153–184
Hartl DL (2000) A primer of population genetics, vol 3rd. Sinauer Associates, Inc. Publishers, Sunderland, pp 70–74
Hauser L, Adcock GJ, Smith PJ, Bernal Ramírez JH, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagus auratus). Proc Natl Acad Sci USA 99:11742–11747
Hoarau G, Piquet AM-T, van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2004) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. J Sea Res 51:183–190
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, vol 29. Springer, Dordrecht, pp 117–178
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:1–6
Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318
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 (2009) Trend in fishery genetics. In: Beamish R, Rothschild B (eds) The future of fisheries science in north America, fish & fisheries series. Springer, Dordrecht, pp 453–493
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
Kochzius M, Seidel C, Hauschild J, Kirchhoff S, Mester P, Meyer-Wachsmuth I, Nuryanto A, Timm J (2009) Genetic population structures of the blue starfish Linckia laevigata and its gastropod ectoparasite Thyca crystallina. Mar Ecol Prog Ser 396:211–219
Kuhnt W, Holbourn A, Hall R, Zuvela M, Käse R (2004) Neogene history of the Indonesian throughflow. In: Clift P, Hayes D, Kuhnt W, Wang P (eds) Continent-ocean interactions in the East Asian marginal seas, vol 149. AGU Monograph, Washington, pp 299–320
Laan M, Pääbo S (1997) Demographic history and linkage disequilibrium in human populations. Nat Genet 17:435–438
Lee JY, Edwards SV (2008) Divergence across Australia’s carpentarian barrier: statistical phylogeography of the red-backed fairy wren (Malurus melanocephalus). Evolution 62:3117–3134
Lourie SA, Green DM, Vincent ACJ (2005) Dispersal, habitat differences, and comparative phylogeography of Southeast Asien seahorses (Syngnathidae: Hippocampus). Mol Ecol 14:1073–1094
Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18:50–60
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Moll H (1983) Zonation and diversity of Scleractinia on reef off S.W. Sulawesi, Indonesia. PhD Thesis, University of Leiden, The Netherlands
Mulligan CJ, Kitchen A, Miyamoto MM (2006) Comment on “populatin size does not influence mitochondrial genetic diversity in animals”. Science 314:1390a
Nauta MJ, Weissing FJ (1996) Constraints on allele size at microsatellite loci: implications for genetic differentiation. Genetics 143:1021–1032
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
Nugroho E, Takagi M, Sugama K, Taniguchi N (1998) Detection of GT repeats microsatellite loci and their polymorphism for grouper of the genus Epinephelus. Fish Sci 64:836–837
Nuryanto A, Kochzius M (2009) Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima. Coral Reefs 28:607–619
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
Planes S, Jones GP, Thorroldd SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci USA 106:5693–5697
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quenouille B, Bouchenak-Khelladi Y, Hervet C, Planes S (2004) Eleven microsatellite loci for the saddleback clownfish Amphiprion polymnus. Mol Ecol Notes 4:291–293
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reilly A, Elliott NG, Grewe PM, Clabby C, Powell R, Ward RD (1999) Genetic differentiation between Tasmanian cultured Atlantic salmon (Salmon salar L.) and their ancestral Canadian population: comparison of microsatellite DNA and allozyme and mitochondrial DNA variation. Aquaculture 173:459–469
Renema W, Troelstra SR (2001) Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeogr Palaeoclimatol Palaeoecol 175:125–146
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
Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419
Ruzzante DE (1998) A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variance. Can J Fish Aquat Sci 55:1–14
Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2009) Estimating connectivity in marine populations: an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios. Mol Ecol 18:1765–1776
Santini S, Polacco G (2006) Finding Nemo: molecular phylogeny and evolution of the unususal life style of anemonefish. Gene 385:19–27
Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid, Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417
Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, New York
Tautz D (1989) Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471
Timm J, Kochzius M (2008) Geological history and oceanography of the Indo-Malay Archipelago shape the 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
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vázquez JF, Pérez T, Albornoz J, Dominguez A (2000) Estimation of microsatellite mutation rates in Drosophila melanogaster. Genet Res 76:323–326
Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and durations. J Biogeogr 27:1153–1167
Wabnitz C, Taylor M, Green E, Razak T (2003) From ocean to aquarium. UNEP-WCMC, Cambridge
Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106
Wares JP, Barber PH, Ross-Ibarra J, Sotka EE, Toonen RJ (2006) Mitochondrial DNA and population size. Science 314:1388–1389
Weber JL, Wong C (1993) Mutation of short tandem repeats. Hum Mol Genet 2:1123–1128
Whitten T, Mustafa M, Henderson GS (2002) The EcOLOGY Of Sulawesi. ecology of Indonesia series, vol IV. Periplus Editions Ltd, Hong Kong
Williams ST (2000) Species boundaries in the starfish genus Linckia. Mar Biol 136:137–148
Wyrtki K (1961) Physical oceanography of the Southeast Asien waters. In: NAGA Report, vol. 2, University of California, Scripps Institution of Oceanography, LaJolla, California
Zavattari P, Deidda E, Whalen M, Lampis R, Mulargia A, Loddo M, Eaves L, Mastio G, Todd JA, Cucca F (2000) Major factors influencing linkage disequilibrium by analysis of different chromosome regions in distinct populations: demography, chromosome recombination frequency and selection. Hum Mol Genet 9:2947–2957
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121
Acknowledgments
We would like to thank the 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 SPICE (Science for the Protection of Indonesian Coastal Marine Ecosystems); Centre for Tropical Marine Ecology (Bremen, Germany) for project co-ordinated, especially C. Richter; GEO Magazine (Hamburg, Germany) for financing the research expedition to Misool and New Guinea; A. Nuryanto from the Jenderal Soedirman University (Purwokerto, Indonesia) for help during field work; colleagues from Universitas Hasanuddin (Makassar, Indonesia) for logistical support during field work in Spermonde Archipelago, especially J. Jompa; the colleagues from the University of Bremen, especially D. Blohm. 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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10592_2012_318_MOESM2_ESM.png
Figure: Genetic structure of a subset of Amphiprion ocellaris populations with over one-third representatives of the “blue cluster” in the Bayesian analysis including all populations, in the study area. Map of the study area with names of the major islands, seas, and sample sites (for abbreviations refer to Table 1). The frequencies of the different clusters (k = 2) from the analysis with the programme STRUCTURE (ver. 2.2., Pritchard et al. 2000) are indicated by blue and light blue in the pie charts. Major surface currents are given by arrows (solid = uni-directional, dashed = reversing with the monsoon seasons). The light grey shading indicates the land area during the Pleistocene maximum sea level low stand of 120 m (after Voris 2000). (PNG 122 kb)
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Timm, J., Planes, S. & Kochzius, M. High similarity of genetic population structure in the false clown anemonefish (Amphiprion ocellaris) found in microsatellite and mitochondrial control region analysis. Conserv Genet 13, 693–706 (2012). https://doi.org/10.1007/s10592-012-0318-1
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DOI: https://doi.org/10.1007/s10592-012-0318-1