Analysis of global and local population stratification of finless porpoises Neophocaena phocaenoides in Chinese waters

Abstract

The existence of three distinct populations is widely accepted for the finless porpoise (Neophocaena phocaenoides) in Chinese waters: the Yellow Sea, Yangtze River, and South China Sea populations. Here, we use nine species-specific microsatellite loci, the complete mitochondrial DNA control region (912 bp), and the complete mitochondrial cytochrome b gene (1,140 bp) to further investigate potential population stratification in the Yellow Sea using 147 finless porpoise samples from the Bohai Sea and adjacent northern Yellow Sea, two regions that were largely underrepresented in previous genetic studies. Our F-statistics analyses confirm the previously described three populations, but further demonstrate significant genetic differentiation between the [Bohai + northern Yellow] Sea and the southern Yellow Sea. On the other hand, median-joining network analyses do not exhibit well-differentiated haplotype groups among different geographic populations, suggesting the existence of shared ancestral haplotypes. Levels of microsatellite diversity are moderate to high (mean H E = 0.794) among the 147 [Bohai + northern Yellow] Sea finless porpoises and no recent bottleneck was detected, whereas mtDNA control region and cytochrome b gene diversity is low to moderate. The microsatellite genotypic and mtDNA haplotypic data also confirm the presence of mother-calf pairs in single-net bycatch cases. The results presented here highlight the necessity to treat the [Bohai + northern Yellow] Sea population (highly impacted by anthropogenic threats) as a separate Management Unit.

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References

  1. Alter SE, Ramirez SF, Nigenda S, Ramirez JU, Bracho LR, Palumbi SR (2009) Mitochondrial and nuclear genetic variation across Calving Lagoons in Eastern North Pacific Gray Whales (Eschrichtius robustus). J Hered 100:34–46. doi:10.1093/jhered/esn090

    Article  CAS  Google Scholar 

  2. Amano M, Miyazaki N, Kureha K (1992) A morphological comparison of skulls of the finless porpoise Neophocaena phocaenoides from the Indian Ocean, Yangtze River, and Japanese waters. J Mammal Soc Jpn 17:59–69

    Google Scholar 

  3. Amaral AR, Sequeira M, Martínez-Cedeira J, Coelho MM (2007) New insights on population genetic structure of Delphinus delphis from the northeast Atlantic and phylogenetic relationships within the genus inferred from two mitochondrial markers. Mar Biol 151:1967–1976. doi:10.1007/s00227-007-0635-y

    Article  Google Scholar 

  4. Baker CS, Weinrich MT, Early G, Palumbi SR (1994a) Genetic impact of an unusual group mortality among Humpback Whales. J Hered 85:52–54

    CAS  Google Scholar 

  5. Baker CS, Slade RW, Bannister JL, Abernethy RB, Weinrich MG, Lien J, Urban J, Corkeron P, Calambokidis J, Vasquez O, Palumbi SR (1994b) Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, world-wide. Mol Ecol 5:283–287

    Google Scholar 

  6. Bandelt H, Forster P, Röhl A (1999) Networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  Google Scholar 

  7. Cassens I, Van Waerebeek K, Best PB, Crespo EA, Reyes J, Milinkovitch MC (2003) The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Mol Ecol 12:1781–1792

    Article  CAS  Google Scholar 

  8. Cassens I, Van Waerebeek K, Best PB, Tzika A, Van Helden AL, Crespo EA, Milinkovitch MC (2005) Evidence for male dispersal along the coasts but no migration in pelagic waters in dusky dolphins (Lagenorhynchus obscurus). Mol Ecol 14:107–121

    Article  Google Scholar 

  9. Chen L, Yang G (2008) Development of tetranucleotide microsatellite loci for the finless porpoise. Conserv Genet 9:1033–1035

    Article  CAS  Google Scholar 

  10. Chen L, Bruford M, Yang G (2007) Isolation and characterization of microsatellite loci in the finless porpoise (Neophocaena phocaenoides). Mol Ecol 17:3078–3094

    Google Scholar 

  11. Chen L, Bruford MW, Xu SX, Zhou KY, Yang G (2010) Microsatellite variation and significant population genetic structure of endangered finless porpoises (Neophocaena phocaenoides) in Chinese coastal waters and the Yangtze River. Mar Biol 157:1453–1462

    Article  Google Scholar 

  12. Chivers SJ, Dizon AE, Gearin P, Robertson KM (2002) Small-scale population structure of eastern North Pacific harbor porpoise, Phoceona phocoena, indicated by molecular genetic analyses. J Cetacean Res Manag 4:111–122

    Google Scholar 

  13. Chivers SJ, Baird RW, McSweeney DJ, Webster DL, Hedrick NM, Salinas JC (2007) Genetic variation and evidence for population structure in eastern North Pacific false killer whales (Pseudorca crassidens). Can J Zool 85:783–794

    Article  CAS  Google Scholar 

  14. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  Google Scholar 

  15. Dalebout ML, Ruzzante DE, Whitehead H, Oien N (2006) Nuclear and mitochondrial markers reveal distinctiveness of a small population of bottlenose whales, Hyperoodon ampullatus, in the western North Atlantic. Mol Ecol 15:3115–3129

    Article  CAS  Google Scholar 

  16. Di Rienzo A, Peterson AC, Garza JC (1994) Mutational processes of simple sequence repeat loci in human populations. PNAS USA 91:3166–3170

    Article  CAS  Google Scholar 

  17. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  Google Scholar 

  18. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  CAS  Google Scholar 

  19. Escorza-Treviño S, Archer FI, Rosales M, Lang A, Dizon AE (2005) Genetic differentiation and intraspecific structure of eastern tropical Pacific spotted dolphins, Stenella attenuata, revealed by DNA analyses. Conserv Genet 6:587–600

    Article  Google Scholar 

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

    CAS  Google Scholar 

  21. Excoffier L, Laval G, Schneider S (2005) Arlequin version 3: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  22. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  Google Scholar 

  23. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  Google Scholar 

  24. Gao AL (1991) Morphological differences and genetic variation among the populations of Neophocaena phocaenoides. Dissertation, Nanjing Normal University, Nanjing (in Chinese, with English Abstr.)

  25. Gao AL, Zhou K (1993) Growth and reproduction of three populations of finless porpoise, Neophocaena phocaenoides, in Chinese waters. Aquat mamm 19:3–12

    Google Scholar 

  26. Gao AL, Zhou KY (1995a) Geographical variation of external measurements and three subspecies of Neophocaena phocaenoides in Chinese waters. Acta Theriol Sinica 15:81–92

    Google Scholar 

  27. Gao AL, Zhou KY (1995b) Geographical variation of skull among the populations of Neophocaena phocaenoides in Chinese waters. Acta Theriol Sinica 15:161–169

    Google Scholar 

  28. Gao AL, Zhou KY (1995c) Geographical variation of postcranial skeleton among the populations of Neophocaena phocaenoides in Chinese waters. Acta Theriol Sinica 15:246–253

    Google Scholar 

  29. Garza JC, Williamson EG (2001) Detecting of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  Google Scholar 

  30. Guan BX (1963) A preliminary study of the temperature variations and the characteristics of the circulation of the Cold Water Mass in Yellow Sea. Oceanologia et Limnologia Sinica 5:255–284 (in Chinese, with English Abstr.)

    Google Scholar 

  31. Guo SW, Thompson EA (1992) Performing the exact test for Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  CAS  Google Scholar 

  32. Hamilton H, Caballero S, Collins AG, Brownell RL Jr (2001) Evolution of river dolphins. Proc R Soc Lond B Biol Sci 268:549–556

    Article  CAS  Google Scholar 

  33. Harwood J (1999) A risk assessment framework for the reduction of cetacean by-catches. Aquat Conserv Mar Freshw Ecosyst 9:593–599

    Article  Google Scholar 

  34. Hayano A, Amano M, Miyazaki N (2003) Phylogeography and population structure of the Dall’s porpoise, Phocoenoides dalli, in Japanese waters revealed by mitochondrial DNA. Genes Genet Syst 78:81–91

    Article  CAS  Google Scholar 

  35. Hoelzel AR, Hancock JM, Dover GA (1991) Evolution of the cetacean mitochondrial D-loop region. Mol Biol Evol 8:475–493

    CAS  Google Scholar 

  36. Jackson JBC (1974) Biogeographic consequences of eurytopy and stenotopy among marine bivalves and their evolutionary significance. Am Nat 108:541–560

    Article  Google Scholar 

  37. Jayasankar P, Anoop B, Rajagopalan M (2008) PCR based sex determination of cetaceans and dugong from the Indian Seas. Curr Sci India 94:1513–1516

    CAS  Google Scholar 

  38. Jefferson TA, Hung SK, Law L, Torey M, Tregenza N (2002) Distribution and abundance of finless porpoises in waters of Hong Kong and adjacent areas of China. Raffles Bull Zool Suppl 10:43–55

    Google Scholar 

  39. Jiang ZJ, Castoe TA, Austin CC, Burbrink FT, Herron MD, McGuire JA, Parkinson CL, Pollock DD (2007) Comparative mitochondrial genomics of snakes: extraordinary substitution rate dynamics and functionality of the duplicate control region. BMC Evol Biol 7:123

    Article  Google Scholar 

  40. Kasuya T (1999) Finless porpoise Neophocaena phocaenoides (G. Guvier, 1829). In: Ridgwag SH, Harrison R (eds) Handbook of marine mammals, volume 6: the second book of dolphins and the porpoises. Academic Press, San Diego, pp 411–442

    Google Scholar 

  41. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29

    Article  Google Scholar 

  42. Knowlton N, Jackson JBC (1993) Inbreeding and outbreeding in marine invertebrates. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago, pp 200–249

    Google Scholar 

  43. Ku FC (2006) No recent gene flow among three subspecies of genus Neophocaena revealed by microsatellite markers. Master thesis, National Sun Yat-Sen University, Kaohsiung

  44. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302

    Article  Google Scholar 

  45. Li YL, Kong XY, Yu ZN, Kong J, Ma S, Chen LM (2009) Genetic diversity and historical demography of Chinese shrimp Feneropenaeus chinensis in Yellow Sea and Bohai Sea based on mitochondrial DNA analysis. Afr J Biotechnol 8:1193–1202

    CAS  Google Scholar 

  46. Li X, Tzika AC, Liu YY, Van Doninck K, ZHU Q, Milinkovitch MC (2010) Preliminary genetic status of the spotted seal Phoca largha in Liaodong Bay based on microsatellite and mitochondrial DNA analyses. Trends Evol Biol 2(e6):33–38

    Google Scholar 

  47. Liu P, Meng XH, Kong J, He YY, Wang QY (2006) Polymorphic analysis of microsatellite DNA in wild populations of Chinese shrimp (Fenneropenaeus chinensis). Aquac Res 37:556–562

    Article  CAS  Google Scholar 

  48. Luca M, Andrew W, Emer R, Patricia R, Andrew R, Jamie C, Tom C (2009) Population structure of short-beaked common dolphins (Delphinus delphis) in the North Atlantic Ocean as revealed by mitochondrial and nuclear genetic markers. Mar Biol 156:821–834

    Article  Google Scholar 

  49. Luikart G, Allendorf FW, Sherwin B, Cornuet J-M (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89(3):238–247

    Article  CAS  Google Scholar 

  50. Mardulyn P, Cassens I, Milinkovitch MC (2009) A comparison of methods for constructing evolutionary networks from intraspecific DNA sequence. In: Bertorelle G, Bruford MW, Hauffe HC, Rizzoli A, Vernesi C (eds) Chapter 5, ‘Population genetics for animal conservation’. Cambridge University Press, Cambridge

    Google Scholar 

  51. Mendez M, Rosenbaum H, Bordino P (2008) Conservation genetics of the franciscana dolphin in Northern Argentina: population structure, by-catch impacts, and management implications. Conserv Genet 9(2):419–435

    Article  Google Scholar 

  52. Mila B, Girman DJ, Kimura M, Smith TB (2000) Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird. Proc R Soc Lond B Biol Sci 267:1033–1040

    Article  CAS  Google Scholar 

  53. Morizur Y, Berrow SD, Tregenza NJC, Couperus AS, Pouvreau S (1999) Incidental catches of marine-mammals in pelagic trawl fisheries of the northeast Atlantic. Fish Res 41:297–307

    Article  Google Scholar 

  54. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  55. Olavarria C (2008) Population structure of Southern Hemisphere humpback whales. Dissertation, University of Auckland, Auckland

  56. Palsboll PJ, Clapham PJ, Matilla DK, Larsen F, Sears R, Siegismund HR, Sigurjonsson J, Vasquez O, Arctander P (1995) Distribution of mtDNA haplotypes in North Atlantic humpback whales: the influence of behaviour on population structure. Mar Ecol Prog Ser 116:1–10

    Article  CAS  Google Scholar 

  57. Piry S, Luikart G, Cornuet J-M (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  58. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  59. Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer

  60. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  Google Scholar 

  61. Reeves RR, Wang JY, Leatherwood S (1997) The finless porpoise, Neophocaena phocaenoides (G. Cuvier 1829): a summary of current knowledge and recommendations for conservation action. Asian Mar Biol 14:111–143

    Google Scholar 

  62. Reeves RR, Collins T, Jefferson TA, Karczmarski L, Laidre K., O’Corry-Crowe G, Rojas-Bracho L, Secchi ER, Slooten E, Smith BD, Wang JY, Zhou K (2008) Neophocaena phocaenoides. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.1. http://www.iucnredlist.org (Downloaded on 01 March 2011)

  63. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  64. Rice DW (1998) Marine mammals of the world: systematics and distribution. Soc Mar Mammal, Special Publication No. 4, p 231

  65. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  Google Scholar 

  66. Rosa S, Milinkovitch MC, Van Waerebeek K, Berck J, Oporto J, Alfaro-Shigueto J, Van Bressem MF, Goodall N, Cassens I (2005) Population structure of nuclear and mitochondrial DNA variation among South American Burmeister’s porpoises (Phocoena spinipinnis). Conserv Genet 6:431–443

    Article  CAS  Google Scholar 

  67. Rosel PE (2003) PCR-based sex determination in Odontocete cetaceans. Conserv Genet 4:647–649

    Article  CAS  Google Scholar 

  68. Rosel PE, France SC, Wang JY, Kocher TD (1999) Genetic structure of harbour porpoise, Phocoena phocoena, populations in the Northwest Atlantic based on mitochondrial and nuclear markers. Mol Ecol 8:S41–S54

    Article  CAS  Google Scholar 

  69. Rozas J, Sánche-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  Google Scholar 

  70. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  71. 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 152:1079–1089

    CAS  Google Scholar 

  72. Sellas AB, Wells RS, Rosel PE (2005) Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins Tursiops truncatus in the Gulf of Mexico. Conserv Genet 6:715–728

    Article  CAS  Google Scholar 

  73. Slatkin M, Excoffier L (1996) Testing for linkage disequilibrium in genotypic data using the expectation-maximization algorithm. Heredity 76:377–383

    Article  Google Scholar 

  74. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  Google Scholar 

  75. Sokal RR, Rohlf FJ (1994) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman WH, New York

    Google Scholar 

  76. Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis for DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  77. Tang Q, Liu H, Mayden R, Xiong B (2006) Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Mol Phylogenet Evol 39(2):347–357

    Article  CAS  Google Scholar 

  78. Tiedemann R, Milinkovitch MC (1999) Culture and genetic evolution in whales. Science 284:2055a

    Article  Google Scholar 

  79. 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

    Article  Google Scholar 

  80. Wang JY, Frasier TR, Yang SC, White BN (2008) Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena). Heredity 101:145–155

    Article  CAS  Google Scholar 

  81. Weinrich MT, Rosenbaum H, Baker C, Blackmer AL, Whitehead H (2006) The influence of maternal lineages on social affiliations among humpback whales (Megaptera novaeangliae) on their feeding grounds in the southern gulf of maine. J Hered 97:226–234

    Article  Google Scholar 

  82. Xia JH, Zheng JS, Wang D (2005) Ex situ conservation status of an endangered Yangtze finless porpoise population, Neophocaena phocaenoides asiaeorientalis, as measured from microsatellites and mtDNA diversity. ICES J Mar Sci 62(8):1711–1716

    Article  CAS  Google Scholar 

  83. Yang G, Ren W, Zhou K, Liu S, Ji G, Yan J (2002) Population genetic structure of finless porpoises, Neophocaena phocaenoides, in Chinese waters. Mar Mamm Sci 18(2):336–347

    Article  Google Scholar 

  84. Yang G, Guo L, Bruford M, Wei FW, Zhou KY (2008) Mitochondrial phylogeography and population history of finless porpoises in Sino-Japanese waters. Biol J Linn Soc 95:193–204

    Article  Google Scholar 

  85. Zhao X, Barlow J, Taylor BL, Pitman RL, Wang K, Wei Z, Stewart BS, Turvey ST, Akamatsu T, Reeves RR (2008) Abundance and conservation status of the Yangtze finless porpoise in the Yangtze River, China. Biol Conserv 141:3006–3018

    Article  Google Scholar 

  86. Zheng JS, Xia JH, He SP, Wang D (2005) Population genetic structure of the Yangtze finless Porpoise (Neophocaena phocaenoides asiaeorientalis): implications for management and conservation. Biochem Genet 43:307–320

    Article  CAS  Google Scholar 

  87. Zheng JS, Liao XL, Tong JG, Du HJ, Milinkovitch MC, Wang D (2008) Development and characterization of polymorphic microsatellite loci in the endangered Yangtze finless porpoise (Neophocaena phocaenoides asiaeorientalis). Conserv Genet 9:1007–1009

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Mu Ma, Yumiao Sun, Cuihua Tao, Yanan Liu, Ting Zhang, Qi Zhao, Can Zhou, Mengxuan Cui, Qinglin Ma, and Xiang Xing for assisting fieldwork, sample collection, and measurements. We thank Chiou-Ju Yao for useful suggestions regarding mtDNA control region experiments and critical comments to the early version of the manuscript. We also thank Daniel Monteyne, Eva D’Amico, Raphaël Helaers, Julien Guglielmini, and Lise-Marie Pigneur for technical help. Funds were provided to QZ by the Third Institute of Oceanography, State Oceanic Administration (HE09701 (1), HE09702 (1)), International Cooperation Department, State Oceanic Administration (HC10701-10(1)), Environmental Protection Department, State Oceanic Administration (HD10301-10(1)), Commonweal Project, State Oceanic Administration, China (201105011) and the Shandong Natural Science Foundation (Y2007D75). Funds were provided to MCM by the University of Geneva, the Georges & Antoine Claraz Foundation (Switzerland), the Ernst & Lucie Schmidheiny Foundation (Switzerland), and the National Fund for Scientific Research Belgium (FNRS). ACT is post-doctoral fellow at the FNRS, Belgium. X. Li is a PhD candidate supported by the Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture (FRIA), Belgium.

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Correspondence to Qian Zhu or Karine Van Doninck.

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Communicated by M. I. Taylor.

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Li, X., Liu, Y., Tzika, A.C. et al. Analysis of global and local population stratification of finless porpoises Neophocaena phocaenoides in Chinese waters. Mar Biol 158, 1791–1804 (2011). https://doi.org/10.1007/s00227-011-1692-9

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Keywords

  • Mismatch Distribution
  • Yangtze River
  • Finless Porpoise
  • Common Dolphin
  • Bayesian Skyline Plot