Molecular phylogeography and population genetic structure of the planktonic copepod <i>Calanus sinicus</i> Brodsky in the coastal waters of China

Huang Yousong; Liu Guangxing; Chen Xiaofeng

doi:10.1007/s13131-014-0542-2

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2014 > 33(10): 74-84

Huang Yousong, Liu Guangxing, Chen Xiaofeng. Molecular phylogeography and population genetic structure of the planktonic copepod Calanus sinicus Brodsky in the coastal waters of China[J]. Acta Oceanologica Sinica, 2014, 33(10): 74-84. doi: 10.1007/s13131-014-0542-2

Citation:

Huang Yousong, Liu Guangxing, Chen Xiaofeng. Molecular phylogeography and population genetic structure of the planktonic copepod Calanus sinicus Brodsky in the coastal waters of China[J]. Acta Oceanologica Sinica, 2014, 33(10): 74-84. doi: 10.1007/s13131-014-0542-2

Citation:

PDF( 820 KB)

Molecular phylogeography and population genetic structure of the planktonic copepod Calanus sinicus Brodsky in the coastal waters of China

doi: 10.1007/s13131-014-0542-2

1.
College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
2.
College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China;Key Laboratory of Marine Environment and Ecology of Ministry of Education, Ocean University of China, Qingdao 266100, China

Received Date: 2013-04-13
Rev Recd Date: 2013-12-17

Abstract

Abstract

Planktonic copepod Calanus sinicus is the dominant meso-zooplankton in the Northwest Pacific Ocean. To better understand its population dynamics and phylogeographic patterns, 243 C. sinicus individuals were collected from seven locations across the shelf waters of China and its population genetics was studied by mitochondrial DNA cytochrome oxidase I (mtCOI) sequences analyses. Thirty-nine different sequences, or haplotypes, were detected with moderate haplotype diversity (h=0.749) and low nucleotide diversity (π=0.003) for all populations. The evolutionary divergence between geographic populations varied from 0.24% to 0.37%, indicative of very limited genetic differentiation. Visualized minimum spanning network (MSN) and phylogenetic analysis of all the detected haplotypes did not reveal any clear phylogeographic pattern. Furthermore, AMOVA data showed no significant spatial population differentiation existed among the individuals collected across China shelf waters. Pairwise F_ST values showed that population collected from northwest of the East China Sea (ECS) displayed a low difference to other populations. Mismatch distribution analyses and neutrality tests indicated that C. sinicus might undergo a demographic/population expansion. No significant population genetic structuring was detected, indicating an extensive gene flow among the C. sinicus populations. Our results provide molecular evidence for the hypothesis that C. sinicus in the northwestern South China Sea in winter is transported from the East China Sea and the Yellow Sea by the China Coastal Current during the northeast monsoon period.
- copepod,
- Calanus sinicus,
- mtCOI,
- population genetic differentiation,
- China Coastal Current

FullText(HTML)

References(71)

References

Asahida T, Yamashita Y, Kobayashi T. 1997. Identification of consumed stone flounder, Kareius bicoloratus (Basilewsky), from the stomach contents of sand shrimp, Crangon affinis (De Haan) using mitochondrial DNA analysis. Journal of Experimental Marine Biology and Ecology, 217(2): 153-163

Atkinson D. 1994. Temperature and organism size-a biological law for ectotherms? Advances in Ecological Research, 25: 1-58

Avise J C. 2000. Phylogeography: the History and Formation of Species. Cambridge: Harvard University Press Avise J C. 2009. Phylogeography: retrospect and prospect. Journal of Biogeography, 36(1): 3-15

Bi Hongsheng, Sun Song, Gao Shangwu, et al. 2001. The ecological characteristics of zooplankton community in the Bohai Sea: II. The distribution of copepoda abundance and seasonal dynamics. Acta Ecologica Sinica (in Chinese), 21(2): 177-185

Blanco-Bercial L, lvarez-Marqués F, Bucklin A. 2011. Comparative phylogeography and connectivity of sibling species of the marine copepod Clausocalanus (Calanoida). Journal of Experimental Marine Biology and Ecology, 404(1-2): 108-115

Boore J L. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767-1780

Boore J L, Fuerstenberg S I. 2008. Beyond linear sequence comparisons: the use of genome-level characters for phylogenetic reconstruction. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1496): 1445-1451

Bradford J M. 1988. Review of the taxonomy of the Calanidae (Copepoda) and the limits to the genus Calanus. Hydrobiologia, 167-168(1): 73-81

Bucklin A, Astthorsson O S, Gislason A, et al. 2000. Population genetic variation of Calanus finmarchicus in Icelandic waters: preliminary evidence of genetic differences between Atlantic and Arctic populations. ICES Journal of Marine Science, 57(6): 1592-1604

Bucklin A, Frost B W, Bradford-Grieve J, et al. 2003. Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Marine Biology, 142(2): 333-343

Bucklin A, Wiebe P H. 1998. Low mitochondrial diversity and small effective population sizes of the copepods Calanus finmarchicus and Nannocalanus minor: possible impact of climatic variation during recent glaciation. Journal of Heredity, 89(5): 383-392

Burton R S, Byrne R J, Rawson P D. 2007. Three divergent mitochondrial genomes from California populations of the copepod Tigriopus californicus. Gene, 403(1-2): 53-59

Cao Wenqing, Lin Yuanshao, Yang Qing, et al. 2006. Advanced in biol ogy of Calanus sinicus in China. Journal of Xiamen University (Natural Science) (in Chinese), 45: 54-61

Chen Gang, Hare M P. 2011. Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast. Molecular Ecology, 20(11): 2425-2441

Chen Hongju, Qi Yanping, Liu Guangxing. 2011. Spatial and temporal variations of macro-and mesozooplankton community in the Huanghai Sea (Yellow Sea) and East China Sea in summer and winter. Acta Oceanologica Sinica, 30(2): 84-95

Chen Qingchao. 1964. A study of the breeding periods, variation in sex ratio and in size of Calanus sinicus Brodsky. Oceanologia et Limnologia Sinica (in Chinese), 6(3): 272-288

Chen Qingchao, Zhang Shuzhen. 1965. The planktonic copepods of the Yellow Sea and the East China Sea: I. Calanoida. Studia Marina Sinica (in Chinese), 7: 1-131

Chen Qingchao. 1992. Zooplankton of China Seas. Beijing: Science Press, 243-254

Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1: 47-50

Excoffier L, Smouse P E, Quattro J M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131(2): 479-491

Folmer O, Black M, Hoeh W, et al. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5): 294-299

Forster J, Hirst A G, Atkinson D. 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences of the United States of America, 109(47): 19310-19314

Han Xifu, Wang Rong, Wang Junping. 2002. Digestive gut structure and activity of protease, amylase, and alkaline phosphatase in Calanus sinicus during summer in the Yellow Sea and the East China Sea. Journal of Experimental Marine Biology and Ecology, 270(2): 131-146

Hirota R. 1964. Zooplankton investigations in Hiuchi-nada in the Setonaikai (Inland Sea of Japan): I. The seasonal occurrence of copepods at the three stations in Hiuchi-nada. Journal of the Oceanographical Society of Japan, 20: 24-31

Hirota R. 1979. Seasonal occurrence of zooplankton at a definite station off Mukaishima from July of 1976 to June of 1977. Publications from the Amakusa Marine Biological Laboratory, 5: 9-17

Hsieh C H, Chen C S, Chiu T S. 2005. Composition and abundance of copepods and ichthyoplankton in Taiwan Strait (western North Pacific) are influenced by seasonal monsoons. Marine and Freshwater Research, 56(2): 153-161

Huang C, Uye S, Onbé T. 1993a. Geographic distribution, seasonal life cycle, biomass and production of a planktonic copepod Calanus sinicus in the Inland Sea of Japan and its neighboring Pacific Ocean. Journal of Plankton Research, 15(11): 1229-1246

Huang C, Uye S, Onbé T. 1993b. Ontogenetic diel vertical migration of the planktonic copepod Calanus sinicus in the Inland Sea of Japan: III. Early summer and overall seasonal pattern. Marine Biology, 117(2): 289-299

Hulsemann K. 1994. Calanus sinicus Brodsky and C. jashnovi, nom. nov. (Copepoda: Calanoida) of the North-west Pacific Ocean: A comparison, with notes on the integumental pore pattern in Calanus s. str. Invertebrate Taxonomy, 8: 1461-1482

Huo Yuanzi, Wang Shiwei, Sun Song, et al. 2008. Feeding and egg production of the planktonic copepod Calanus sinicus in spring and autumn in the Yellow Sea, China. Journal of Plankton Research, 30(6): 723-734

Hwang J S, Wong C K. 2005. The China Coastal Current as a driving force for transporting Calanus sinicus (Copepoda: Calanoida) from its population centers to waters off Taiwan and Hong Kong during the winter northeast monsoon period. Journal of Plankton Research, 27(2): 205-210

Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2): 111-120

Knowlton N. 2000. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia, 420(1): 73-90

Kozol R, Blanco-Bercial L, Bucklin A. 2012. Multi-gene analysis reveals a lack of genetic divergence between Calanus agulhensis and Calanus sinicus (Copepoda; Calanoida). PLoS ONE, 7(10): e45710

Kumar S, Nei M, Dudley J, et al. 2008. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9(4): 299-306

Larkin M A, Blackshields G, Brown N P, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21): 2947-2948

Lee C E. 2000. Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate "populations". Evolution, 54(6): 2014-2027

Lee H J, Chao S Y, 2003. A climatological description of circulation in and around the East China Sea. Deep-Sea Research Part II: Topical Studies in Oceanography, 50(6-7): 1065-1084

Li Chaolun, Sun Song, Wang Rong, et al. 2004. Feeding and respiration rates of a planktonic copepod (Calanus sinicus) oversummering in Yellow Sea Cold Bottom Waters. Marine Biology, 145(1): 149-157

Li Jie, Sun Song, Li Chaolun, et al. 2006. Effects of single and mixed diatom diets on the reproduction of copepod Calanus sinicus. Acta Hydrochimica Et Hydrobiologica, 34(1-2): 117-125

Li Naisheng, Zhao Songling, Wasiliev B. 2000. Geology of Marginal Sea in the Northwest Pacific (in Chinese). Harbin: Heilongjiang Education Press Lin Yuanshao, Fang Lüping, Cao Wenqing, et al. 2005. Mitochodrial DNA COI sequence analysis of Calanus sinicus (Copepod) in Qingdao waters. Journal of Xiamen University (Natural Science) (in Chinese), 44(1): 90-93

Liu Jinxian, Gao Tianxiang, Wu Shifang, et al. 2007. Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Molecular Ecology, 16(2): 275-288

Meng Tianxiang. 2003. Studies on the feeding of anchovy (Engraulis japonicus) at different life stages on zooplankton in the Middle and Southern Waters of the Yellow Sea. Marine Fisheries Research (in Chinese), 24(3): 1-9

Milligan P J, Stahl E A, Schizas N V, et al. 2011. Phylogeography of the copepod Acartia hudsonica in estuaries of the northeastern United States. Hydrobiologia, 666(1): 155-165

Nei M. 1987. Molecular Evolutionary Genetics. New York: Columbia University Press, 1-448

Nelson R J, Carmack E C, Mclaughlin F A, et al. 2009. Penetration of Pacific zooplankton into the western Arctic Ocean tracked with molecular population genetics. Marine Ecology Progress Series, 381: 129-138

Nonomura T, Machida R J, Nishida S. 2008. Stage-V copepodites of Calanus sinicus and Calanus jashnovi (Copepoda: Calanoida) in mesopelagic zone of Sagami Bay as identified with genetic markers, with special reference to their vertical distribution. Progress in Oceanography, 77(1): 45-55

Nuwer M L, Frost B W, Armbrust E V. 2008. Population structure of the planktonic copepod Calanus pacificus in the North Pacific Ocean. Marine Biology, 156(2): 107-115

Papadopoulos L N, Peijnenburg K T C A, Luttikhuizen P C. 2005. Phylogeography of the calanoid copepods Calanus helgolandicus and C. euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. Marine Biology, 147(6): 1353-1365

Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25(1): 1253-1256

Provan J, Beatty G E, Keating S L, et al. 2009. High dispersal potential has maintained long-term population stability in the North Atlantic copepod Calanus finmarchicus. Proceedings of the Royal Society B: Biological Sciences, 276(1655): 301-307

Pu Xinming, Sun Song, Yang Bo, et al. 2004. Life history strategies of Calanus sinicus in the southern Yellow Sea in summer. Journal of Plankton Research, 26(9): 1059-1068

Rohlf F J. 1973. Algorithm 76. Hierarchical clustering using the minimum spanning tree. Computer Journal, 16: 93-95

Shui Bonian, Han Zhiqiang, Gao Tianxiang, et al. 2009. Mitochondrial DNA variation in the East China Sea and Yellow Sea populations of Japanese Spanish mackerel Scomberomorus niphonius. Fisheries Science, 75(3): 593-600

Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3): 585-595

Tan Shuhui, Lin Yuanshao, Cao Wenqing, et al. 2003. Studies on population genetics of Calanus sinicus (Copepod) in Yellow Sea and the East China Sea: I. Allozyme analysis. Journal of Xiamen Uiniversity (Natural Science) (in Chinese), 42(1): 87-91

Uye S. 1988. Temperature-dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia, 167-168(1): 285-293

Uye S. 2000. Why does Calanus sinicus prosper in the shelf ecosystem of the Northwest Pacific Ocean? ICES Journal of Marine Science, 57: 1850-1855

Uye S, Huang C, Onbe T. 1990. Ontogenetic diel vertical migration of the planktonic copepod Calanus sinicus in the Inland Sea of Japan. Marine Biology, 104(3): 389-396

Wang Minxiao. 2010. Application of molecular markers to the researches on pelagic copepods in the Chinese coastal regions [dissertation]. Beijing: Chinese Academy of Sciences Wang Minxiao, Sun Song, Li Chaolun, et al. 2011. Distinctive mitochondrial genome of Calanoid copepod Calanus sinicus with multiple large non-coding regions and reshuffled gene order: Useful molecular markers for phylogenetic and population studies. BMC Genomics, 12: 73, doi: 10.1186/1471-2164-12-73

Wang Pinxian. 1999. Response of Western Pacific marginal seas to glacial cycles: paleoceanographic and sedimentological features. Marine Geology, 156(1-4): 5-39

Wang Rong, Zuo Tao, Wang Ke. 2003. The Yellow Sea Cold Bottom Water: An oversummering site for Calanus sinicus (Copepoda, Crustacea). Journal of Plankton Research, 25(2): 169-183

Wang Shiwei, Li Chaolun, Sun Song, et al. 2009. Spring and autumn reproduction of Calanus sinicus in the Yellow Sea. Marine Ecology Progress Series, 379: 123-133

Xu Xuedong, Oda M. 1999. Surface-water evolution of the eastern East China Sea during the last 36,000 years. Marine Geology, 156(1-4): 285-304

Xu Zhaoli, Chen Bijuan. 2007. Seasonal distribution of Calanus sinicus (Copepoda, crustacea) in the East China Sea. Acta Oceanologica Sinica, 26(3): 150-159

Xu Zhaoli, Ma Zhengling, Wu Yumei. 2011. Peaked abundance of Calanus sinicus earlier shifted in the Changjiang River (Yangtze River) Estuary: a comparable study between 1959, 2002 and 2005. Acta Oceanologica Sinica, 30(3): 84-91

Yin Jianqiang, Huang Liangmin, Li Kaizhi, et al. 2011. Abundance distribution and seasonal variations of Calanus sinicus (Copepoda: Calanoida) in the northwest continental shelf of South China Sea. Continental Shelf Research, 31(14): 1447-1456

Yoshida T, Toda T, Kuwahara V, et al. 2004. Rapid response to changing light environments of the calanoid copepod Calanus sinicus. Marine Biology, 145(3): 505-513

Yoshiki T, Yamanoha B, Kikuchi T, et al. 2008. Hydrostatic pressure-induced apoptosis on nauplii of Calanus sinicus. Marine Biology, 156(2): 97-106

Zhang Guangtao, Li Chaolun, Sun Song, et al. 2006. Feeding habits of Calanus sinicus (Crustacea : Copepoda) during spring and autumn in the Bohai Sea studied with the herbivore index. Scientia Marina, 70(3): 381-388

Zhang Wuchang, Tang Danling, Yang Bo, et al. 2009. Onshore-offshore variations of copepod community in northern South China Sea. Hydrobiologia, 636(1): 257-269

Relative Articles

Supplements(0)

Cited By

Proportional views