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Cryptic genetic divergence in Scolopsis taenioptera (Perciformes: Nemipteridae) in the western Pacific Ocean

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Abstract

We studied the phylogeny, population structure, and demographic history of Scolopsis taenioptera in the western Pacific Ocean. Using the 80 samples collected from four locations, we obtained the nucleotide sequences of mitochondrial cytochrome c oxidase subunit I and cytochrome b genes. We identified two distinct lineages showing a clear phylogeographic break that was possibly due to the Pleistocene sea-level change. One lineage was distributed in Iloilo (Philippines) and the other in Terengganu (Malaysia), Rayong (Thailand), and Ha Long Bay (Vietnam). The Terengganu and Rayong populations showed clear signs of demographic expansion; the Iloilo and Ha Long Bay populations were relatively stable or spatially expanded as geographically subdivided populations.

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References

  • Academia Sinica (2008) Cryobanking Program for Wildlife Genetic Material in Taiwan. http://cryobank.sinica.edu.tw/eng/. Accessed 19 May 2017

  • Amante C, Eakins BW (2009) ETOPO1 1 arc-minute global relief model: procedures, data sources and analysis. NOAA Technical Memorandum NESDIS NGDC-24. National Geophysical Data Center, Boulder

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line? Nature 406:692–3

  • Béarez P (2003) First record of Scolopsis taeniopterus (Nemipteridae) and Gymnocranius elongatus (Lethrinidae) from New Caledonia. Cybium 27:61–62

  • Bellwood DR, Meyer CP (2009) Searching for heat in a marine biodiversity hotspot. J Biogeogr 36:569–576

  • Bellwood DR, Wainwright PC (2002) The History and Biogeography of Fishes on Coral Reefs. In: Sale PF (ed) Coral Reef Fishes. Academic Press, New York, pp 5–32

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 57:289–300

  • Bivand R, Lewin-Koh N (2017) maptools: tools for reading and handling spatial objects v0.9-1. https://CRAN.R-project.org/package=maptools. Accessed 17 March 2017

  • Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537

  • Briggs JC (1999) Coincident biogeographic patterns: Indo-West Pacific Ocean. Evolution 53:326–335

  • Carpenter KE, Niem VH (eds) (2001) The Living Marine Resources of the Western Central Pacific. Vol 5. FAO, Rome

  • Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environ Biol Fishes 72:467–480

  • Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto, Mahardika GN, Manjaji-Matsumoto BM, Juinio-Meñez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol 2011:1–14

  • Cowman PF, Bellwood DR, Rocha LA (2013) The historical biogeography of coral reef fishes: global patterns of origination and dispersal. J Biogeogr 40:209–224

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–92

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–7

  • Fleminger A (1986) The Pleistocene equatorial barrier between the Indian and Pacific Oceans and a likely cause for Wallace’s line. UNESCO Tech Pap Mar Sci 49:84–97

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–25

  • Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648

  • Grant WS (2015) Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. J Hered 106:333–46

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

  • Guo Y, Wang Z, Liu C, Liu L, Liu Y (2007) Phylogenetic relationships of South China Sea snappers (genus Lutjanus; family Lutjanidae) based on mitochondrial DNA sequences. Mar Biotechnol 9:682–8

  • Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the sunda shelf: A late-glacial sea-level record. Science 288:1033–5

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

  • Hess PN, Russo CAM (2007) An empirical test of the midpoint rooting method. Biol J Linn Soc 92:669–674

  • Hung K-W, Russell BC, Chen W-J (2017) Molecular systematics of threadfin breams and relatives (Teleostei, Nemipteridae). Zool Scr. doi 10.1111/zsc.12237

  • Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

  • Lanfear R, Calcott B, Ho SY, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–701

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

  • Leigh JW, Susko E, Baumgartner M, Roger AJ (2008) Testing congruence in phylogenomic analysis. Systmatic Biology 57:104–15

  • Lessios HA (2008) The Great American Schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu Rev Ecol Evol Syst 39:63–91

  • Lourie SA, Vincent ACJ (2004) A marine fish follows Wallace’s Line: the phylogeography of the three-spot seahorse (Hippocampus trimaculatus, Syngnathidae, Teleostei) in Southeast Asia. J Biogeogr 31:1975–1985

  • Lourie SA, Green DM, Vincent AC (2005) Dispersal, habitat differences, and comparative phylogeography of Southeast Asian seahorses (Syngnathidae: Hippocampus). Mol Ecol 14:1073–94

  • Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proc R Soc B 279:1033–40

  • McManus JW (1985) Marine speciation, tectonics and sea-level changes in Southeast Asia. Proc Fifth Int Coral Reef Cong, Tahiti 4:133–138

  • Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78

  • Muto N, Alama UB, Hata H, Guzman AMT, Cruz R, Gaje A, Traifalgar RFM, Kakioka R, Takeshima H, Motomura H, Muto F, Babaran RP, Ishikawa S (2016) Genetic and morphological differences among the three species of the genus Rastrelliger (Perciformes: Scombridae). Ichthyol Res 63:275–287

  • Orrell TM, Carpenter KE, Musick JA, Graves JE (2002) Phylogenetic and biogeographic analysis of the Sparidae (Perciformes: Percoidei) from cytochrome b sequences. Copeia 2002:618–631

  • Otto-Bliesner BL, Schneider R, Brady EC, Kucera M, Abe-Ouchi A, Bard E, Braconnot P, Crucifix M, Hewitt CD, Kageyama M, Marti O, Paul A, Rosell-Melé A, Waelbroeck C, Weber SL, Weinelt M, Yu Y (2009) A comparison of PMIP2 model simulations and the MARGO proxy reconstruction for tropical sea surface temperatures at last glacial maximum. Clim Dyn 32:799–815

  • Pante E, Simon-Bouhet B (2013) marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One 8:e73051

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–20

  • R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

  • Rambaut A (2014) FigTree v1.4.2. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 1 September 2015

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 11 November 2015

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–100

  • Ratnasingham S, Hebert PD (2007) BOLD: the barcode of life data system. http://www.barcodinglife.org. Mol Ecol Notes 7:355–364

  • Ravago-Gotanco RG, Juinio-Meñez MA (2010) Phylogeography of the mottled spinefoot Siganus fuscescens: Pleistocene divergence and limited genetic connectivity across the Philippine archipelago. Mol Ecol 19:4520–34

  • Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–69

  • 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 95:315–26

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–42

  • Sale PF (2004) Connectivity, recruitment variation, and the structure of reef fish communities. Integr Comp Biol 44:390–9

  • Sanciangco MD, Rocha LA, Carpenter KE (2011) A molecular phylogeny of the Grunts (Perciformes: Haemulidae) inferred using mitochondrial and nuclear genes. Zootaxa 2966:37–50

  • Sanderson MJ, Shaffer HB (2002) Troubleshooting molecular phylogenetic analyses. Annu Rev Ecol Syst 33:49–72

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–89

  • Schnute JT, Boers N, Haigh R (2015) PBSmapping: mapping fisheries data and spatial analysis tools v2.69.76. https://CRAN.R-project.org/package=PBSmapping. Accessed 1 December 2015

  • Sevilla RG, Diez A, Norén M, Mouchel O, Jérôme M, Verrez-Bagnis V, Van Pelt H, Favre-Krey L, Krey G, The Fishtrace Consortium, Bautista JM (2007) Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Mol Ecol Notes 7:730–734

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–62

  • Song CB, Near TJ, Page LM (1998) Phylogenetic relations among percid fishes as inferred from mitochondrial cytochrome b DNA sequence data. Mol Phylogenet Evol 10:343–53

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–3

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–95

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–9

  • Yearsley GK, Last PR, Ward RD (1999) Australian Seafood Handbook: an identification guide to domestic species. CSIRO Marine Research, Hobart

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Acknowledgements

The authors thank Mahyam M. I., Raja Bidin R. H., M. Katoh, O. Abe (Marine Fishery Resources Development and Management Department, Southeast Asian Fisheries Development Center, Kuala Terengganu, Malaysia), Seah Y. G., Mazlan A. G. (Universiti Malaysia Terengganu), Aziz A. (Universiti Putra Malaysia), V. Vilasri (Natural History Museum, National Science Museum, Bangkok, Thailand), Chien P.V., Nhan D.V., Chien V.V. (Institute of Marine Environment and Resources, Hai Phong, Vietnam), S. Kimura, Y. Hibino, H. Suzuki (Mie University), M. Nakae, K. Matsuura (National Museum of Nature and Science, Tokyo, Japan), H. Imamura (Hokkaido University), T. Yoshida, Jeong B., S. Tashiro (Kagoshima University), A. Takagi, Yap M. and Y. Ogata (Research Institute for Humanity and Nature, Kyoto, Japan; RIHN) for their help in sampling and arrangements. This study was conducted under a Memorandum of Agreement for joint research made by and among the Department of Agriculture of the Republic of the Philippines (DA), University of the Philippines Visayas (UPV), Kagoshima University Museum, RIHN and Tokai University, facilitated by S. L. Sanchez [Bureau of Fisheries and Aquatic Resources (BFAR), DA]. P.J. Alcala (DA) provided a Prior Informed Consent Certificate, and I.P. Cabacaba and S.M.S. Nolasco (BFAR, DA) provided a Fish Specimen Export Certificate (no. 2016-39812). We thank the staff of the Office of the Vice-Chancellor for Research and Extension, UPV, and the UPV Museum of Natural Sciences, College of Fisheries, UPV, including S.S. Garibay, V.G. Urbina, L.H. Mooc, C.J.N. Rubido and E.P. Abunal, and graduate students of the College of Fisheries, UPV for their support of this research collaboration. Malaysian specimens were collected during the Japan Society for the Promotion of Science (JSPS), Tokyo Asian Core Program, ‘Establishment of Research and Education Network on Coastal Marine Science in Southeast Asia’, supported by the Ministry of Higher Education, Putrajaya, Universiti Putra Malaysia and Universiti Malaysia Terengganu. The Thai specimens were collected with the supports of the Training Department, Southeast Fisheries Development Center, Bangkok, and the Eastern Marine and Research Center, Rayong. The Vietnamese specimens were collected with the support of the Institute of Marine Environment and Resources, and the Ha Long Bay Management Department and with a permission of use of the specimens by the Biodiversity Conservation Agency, Ministry of Natural Resources and Environment, Vietnam. This study was supported by the projects ‘Coastal Area Capability Enhancement in Southeast Asia’ of RIHN (no. 14200061) and ‘Biological Properties of Biodiversity Hotspots in Japan’ of the National Museum of Nature and Science, the JSPS Asian Core Program ‘Establishment of Research and Education Network on Coastal Marine Science in Southeast Asia’, Grants-in-Aid for Scientific Research (C:26450265) and Young Scientists (B:26840131) from JSPS, the fund for international collaboration (NDT.16 TW/16; VAST04.08/17-18) from the Ministry of Science and Technology, Hanoi, and Vietnam Academy of Science and Technology Grant in Marine Sciences and Technology (VAST 06.04/18-19).

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Author notes

  1. Ryo Kakioka

    Present address: Division of Ecological Genetics, National Institute of Genetics, 1111 Yata, Mishima, 411-8540, Japan

  2. Nozomu Muto

    Present address: School of Biological Sciences, Tokai University, 1-1-1 Minamisawa-5-Jo, Minami ku, Sapporo, 005-8601, Japan

Authors and Affiliations

  1. Research Institute for Humanity and Nature, 457-4 Kamigamo-Motoyama, Kita ku, Kyoto, 603-8047, Japan

    Ryo Kakioka, Nozomu Muto, Hirohiko Takeshima & Satoshi Ishikawa

  2. College of Fisheries and Ocean Sciences, University of the Philippines Visayas, Miagao, 5023, Iloilo, Philippines

    Arnold C. Gaje, Ramon S. Cruz, Ulysses B. Alama, Armi May T. Guzman, Rex Ferdinand M. Traifalgar & Ricardo P. Babaran

  3. College of Arts and Sciences, University of the Philippines Visayas, Miagao, 5023, Iloilo, Philippines

    Arnold C. Gaje

  4. Marine Fishery Resources Development and Management Department, Southeast Asian Fisheries Development Center, Taman Perikanan Chendering, 21080, Kuala Terengganu, Malaysia

    Osman Muda & Wahidah Mohd Arshaad

  5. Training Department, Southeast Asian Fisheries Development Center, P.O. Box 97, Phra Samut Chedi, Samut Prakan, 10290, Thailand

    Sukchai Arnupapboon

  6. Eastern Marine Fisheries Research and Development Center, 2 Moo 2, Tambon Phe, Mueang Rayong, Rayong, 21160, Thailand

    Kamolrat Phuttharaksa

  7. Institute of Marine Environment and Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Str., Cau Giay, Hanoi, Vietnam

    Quan Van Nguyen & Thu The Pham

  8. The Kagoshima University Museum, 1-21-30 Korimoto, Kagoshima, 890-0065, Japan

    Hiroyuki Motomura

  9. School of Marine Science and Technology, Tokai University, 3-20-1 Orido, Shimizu ku, Shizuoka, 424-8610, Japan

    Fumihito Muto

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  1. Ryo Kakioka
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Correspondence to Ryo Kakioka.

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Kakioka, R., Muto, N., Takeshima, H. et al. Cryptic genetic divergence in Scolopsis taenioptera (Perciformes: Nemipteridae) in the western Pacific Ocean. Ichthyol Res 65, 92–100 (2018). https://doi.org/10.1007/s10228-017-0596-1

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