Abstract
Ostracods (Crustacea, Ostracoda) are small bivalved crustaceans, contributing to the marine zooplankton community. They are widely distributed and are relatively abundant components of the marine mesozooplankton worldwide, playing an important role in the transport of organic matter to deep layers. By analysing the mitochondrial COI gene, we explored the population genetic structure and haplotype pattern of Porroecia spinirostris which is the dominant ostracod in the South China Sea. We investigated the population genetic structure of ostracods at medium spatial scales in the absence of physical barriers. Our data provides evidence of the importance of both long-distance dispersal as well as genetic isolation in determining the seascape genetic structure of this species. Our data suggest that P.spinirostris can achieve long distance dispersal and specific haplotypes were successful in colonizing habitats from the Xisha to the Nansha area. A total of 36 haplotypes were defined from 85 individuals with most of these haplotypes occurring only once. The dominant haplotype was found in twelve sampling sites. The largest distance between two sampling sites harbouring this haplotype is more than 700 km. Our findings of long distance dispersal in the South China Sea combined with mild genetic differentiation among fifteen sampling sites (average ΦST = 0.167) are in line with a scenario where population genetic structure is strongly impacted by colonization patterns. The seascape genetic structure of P.spinirostris in the South China Sea reflects both the importance of long distance dispersal as well as of reduced levels of gene flow, likely caused by colonization events followed by demographic expansions.
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Angel MV, Blachowiak-Samolyk K, Drapun I, Castillo R (2007) Changes in the composition of planktonic ostracod populations across a range of latitudes in the North-east Atlantic. Prog Oceanogr 73(1):60–78
Angel MV (1983) A review on the progress of research on halocyprid and other oceanic planktonic ostracods1972-1982. In: Maddocks RF (ed) Applications of Ostracoda. Geoscience Department, University of Houston, Houston, pp 529–548
Angel MV (1993) Marine planktonic ostracods: keys and notes for identification of the species. The Linnean Society of London and the Estuarine and Coastal Sciences Association, London, 240 p
Baratti M, Messana GG (2005) High level of genetic differentiation in the marine isopod Sphaeroma terebrans (Crustacea Isopoda Sphaeromatidae) as inferred by mitochondrial DNA analysis. J Exp Mar Biol Ecol 315(2):225–234
Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627
Bilton DT, Freeland J, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Evol S 32:159–181
Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832
Brautovic I, Bojanic N, Batistic M, Caric M (2006). Annual variability of planktonic ostracods (crustacea) in the South Adriatic Sea. Mar Ecol 27(2):124–132
Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Evol S 27:477–500
Cassone BJ, Boulding EG (2006) Genetic structure and phylogeography ofthe lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts. Mar Biol 149:213–226
Castelin M, Feutry P, Hautecoeur M, Marquet G, Wowor D, Zimmermann G, Keith P (2013) New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (fabricius, 1798) (Crustacea: Cecapoda: Palaemonidae). Mar Biol 160(6):1395–1406
Chavtur VG, Bashmanov AG (2015) The composition and distribution of pelagic ostracods (Ostracoda: myodocopa) in the Sea of Japan. Russ J Mar Biol 41(4):250–259
Chen RX, Lin JH (1995) Planktonic ostracoda in China Seas. China Ocean Press, Beijing, 134 p (in Chinese)
Chen RX, Lin JH (1997) Diversity of species and ecological groups of planktonic Ostracoda. Chin Biodivers 5:257–262 (in Chinese)
Chen RX, Lin JH (1998) Large-scale ecological study on planktonic Ostracoda in China seas and adjacent waters. Correlation between planktonic Ostracoda and water systems. Acta Oceonal Sin 20(2):96–101 (in Chinese)
Claremont M, Williams ST, Barraclough TG, Reid DG (2011) The geographic scale of speciation in a marine snail with high dispersal potential. J Biogeogr 38:1016–1032
Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE (2007) Population connectivity in marine systems: an overview. Oceanography 20:14–21
De Meester L, Gomez A, Okamura B, Schwenk K (2002) The monopolisation hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol 23:121–135
De Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J (1999) Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. P Natl Acad Sci USA 96:2864–2868
De Woody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56:461–473
Drapun I, Smith SL (2012) Halocyprid ostracods of the Arabian Sea region. Sultan Qaboos University, Academic Publication Press, Muscat, 223 p
Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493
Ellis CD, Hodgson DJ, Daniels CL, Collins M, Griffiths AG (2017) Population genetic structure in European lobsters: implications for connectivity, diversity and hatchery stocking. Mar Ecol- Prog Ser 563:123–137
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Fang G, Fang W, Fang Y, Wang K (1998) A survey of studies on the south china sea upper ocean circulation. Acta Oceanogr Taiwan 37(1):1–16
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299
Goetze E (2003) Cryptic species on the high seas: global phylogenetics of the copepod family Eucalanidae. P Roy Soc Lond B Bio 270:2321–2331
Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E.spinifer. Evolution 59:2378–2398
Guo WL, Wang LG, Du FY, Jiang SJ (2015) Ecological characteristics of planktonic ostracods in the Nansha Islands waters in spring and autumn. J Fish China 39(6):836–845 (in Chinese)
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98
Han ZQ, Zhu WB, Zheng W, Li PF, Shui BO (2015) Significant genetic differentiation between the Yellow Sea and East China Sea populations of cocktail shrimp Trachypenaeus curvirostris revealed by the mitochondrial DNA COI gene. Biochem Syst Ecol 59:78–84
Haye PA, Segovia NI, Muñozherrera NC, Gálvez FE, Martínez A, Meynard A, Pardo-Gandarillas MC, Poulin E, Faugeron S (2014) Phylogeographic structure in benthic marine invertebrates of the southeast pacific coast of Chile with differing dispersal potential. PLoS One 9(2):e88613
Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol S 40:291–310
Horne JB, Van Herwerden L, Choat JH, Robertson DR (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol 49:629–638
Kaplun NL, Mazdygan ER, Chavtur VG, Gorbatenko KM, Bashmanov AG (2015) Changes in the frequency of the occurrence and abundance of ostracods (ostracoda: halocyprididae) in the epipelagic zone of the north pacific. Russ J Mar Biol 41(3):157–166
Kenchington EL, Patwary MU, Zouros E, Bird CJ (2006) Genetic differentiation in relation to marine landscape in a broadcast spawning bivalve mollusc (Placopecten magellanicus). Mol Ecol 15:1781–1796
Kirby RR, Lindley JA, Batten SD (2007) Spatial heterogeneity and genetic variation in the copepod Neocalanus cristatus along two transects in the North Pacific sampled by the Continuous Plankton Recorder. J Plankton Res 29:97–106
Klinbunga S, Khetpu K, Khamnamtong B, Menasveta P (2007) Genetic heterogeneity of the blue swimming crab (Portunus pelagicus) in Thailand determined by AFLP analysis. Biochem Genet 45:725–736
Kornicker LS (1961) Ecology and taxonomy of recent Bairdiinae (Ostracoda). Micropaleontology 7(1):55–70
Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods Littorina spp. with and without pelagic larval dispersal. Mar Biol 137:835–845
Lee CE (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate ‘populations’. Evolution 54:2014–2027
Lord C, Lorion J, Dettai A, Watanabe S, Tsukamoto K, Cruaud C, Keith P (2012) From endemism to widespread distribution: phylogeography of three amphidromous Sicyopterus species (Teleostei: Gobioidei: Sicydiinae). Mar Ecol-Prog Ser 455:269–285
Ma HY, Ma CY, Li CH, Lu JX, Zou X, Gong YY, Wang W, Chen W, Ma LB, Xia LJ (2015) First mitochondrial genome for the red crab (Charybdis feriata) with implication of phylogenomics and population genetics. Sci Rep-UK 5:11524
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Martens K, Schön I, Meisch C, Horne DJ (2008) Global diversity of ostracods (Ostracoda, Crustacea) in freshwater. Hydrobiologia 595:185–193
Morton B, Blackmore G (2001) South China Sea. Mar Pollut Bull 42:1236–1263
Norris RD (2000) Pelagic species diversity, biogeography and evolution. Paleobiology 26:236–258
Nosil P, Egan SP, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: ‘isolationby- adaptation’ and multiple roles for divergent selection. Evolution 62:316–336
Oakley TH, Wolfe JM, Lindgren AR, Zaharoff AK (2012) Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and pancrustacean phylogeny. Mol Biol Evol 30(1):215–233
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2015) Vegan: community ecology package. http://CRAN.Rproject.org/package=vegan Accessed 10 Dec 2012
Orsini L, Vanoverbeke J, Swillen I, Mergeay J, De Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol 22:5983–5999
Palumbi SR (1992) Marine speciation on a small planet. Trends Ecol Evol 7:114–118
Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Evol S 25:547–572
Papetti C, Zane L, Bortolotto E, Bucklin A, Patarnello T (2005) Genetic differentiation and local temporal stability of population structure in the euphausiid Meganyctiphanes norvegica. Mar Ecol-Prog Ser 289:225–235
Provan J, Beatty GE, Keating SL, Maggs CA, Savidge G (2009) High dispersal potential has maintained long-term population stability in the North Atlantic copepod Calanus finmarchicus. P Roy Soc B-Biol Sci 276:301–307
Ren G, Miao G, Ma C, Lu J, Yang X, Ma H (2018) Genetic structure and historical demography of the blue swimming crab (Portunus pelagicus) from southeastern sea of china based on mitochondrial COI gene. Mitochondrial DNA A 29(2):192–198
Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends Ecol Evol 29:165–176
Rose CG, Paynter KT, Hare MP (2006) Isolation by distance in the Eastern oyster, Crassostrea virginica, in Chesapeake Bay. J Hered 97:158–170
Ruppert EE, Fox RS, Barnes RD (2004) Crustacea. In: Rose N (ed) Invertebrate zoology: a functional evolutionary approach, 7rd edn. Cengage Learning, Belmont, pp 687–690
Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963
Scheltema RS (1986) On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. B Mar Sci 39:290–322
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdana ZA, Finlayson M, Halpern BS, Jorge MA, Lombana AL, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57(7):573–583
Unal E, Bucklin A (2010) Basin-scale population genetic structure of the planktonic copepod Calanus finmarchicus in the North Atlantic Ocean. Prog Oceanogr 87:175–185
Wang IJ, Glor RE, Losos JB (2013) Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol Lett 16:175–182
Werth S, Wagner HH, Gugerli F, Holderegger R, Csencsics D, Kalwij JM, Scheidegger C (2006) Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87:2037–2046
Winters KL, van Herwerden L, Choat JH, Robertson D (2010) Phylogeography of the Indo-Pacific parrotfish Scarus psittacus: isolation generates distinctive peripheral populations in two oceans. Mar Biol 157:1679–1691
White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. P Roy Soc B-Biol Sci 277:1685–1694
Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gerard K, Nadaoka K (2009) Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18:1574–1590
Yang H, Liu Q, Liu Z, Wang D, Liu X (2002) A general circulation model study of the dynamics of the upper ocean circulation of the South China Sea. J Geophys Res-Oceans 107(C7):22–1–22–14
Yin JQ, Chen QC (1991) Planktonic Ostracoda in Nansha archipelago (1984-1988). In: Nansha Scientific Investigation Team (ed) Zooplankton in Nansha archipelago and adjacent waters research study, 2nd edn. Ocean Press, Beijing, pp 64–134 (in Chinese)
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Xu, L., Li, H., Wang, L. et al. Genetic Structure and Haplotype Pattern of Marine Planktonic Ostracod (Porroecia spinirostris) from South China Sea Based on Mitochondrial COI Gene. Ocean Sci. J. 54, 107–116 (2019). https://doi.org/10.1007/s12601-018-0057-4
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DOI: https://doi.org/10.1007/s12601-018-0057-4