Marine Biology

, Volume 156, Issue 8, pp 1573–1583

Genetic diversity and population structure of the Chinese mitten crab Eriocheir sinensis in its native range

  • Liying Sui
  • Fumin Zhang
  • Xiaomei Wang
  • Peter Bossier
  • Patrick Sorgeloos
  • Bernd Hänfling
Original Paper

Abstract

The Chinese mitten crab Eriocheir sinensis is an indigenous and economically important species in China, but can also be found as invasive species in Europe and America. Mitten crabs have been exploited extensively as a food resource since the 1990s. Despite its ecological and economic importance, the genetic structure of native mitten crab populations is not well understood. In this paper, we investigated the genetic structure of mitten crab populations in China by screening samples from ten locations covering six river systems at six microsatellite loci. Our results provide further evidence that mitten crabs from the River Nanliujiang in Southern China are a genetically differentiated population within the native range of Eriocheir, and should be recognized as a separate taxonomic unit. In contrast, extremely low levels of genetic differentiation and no significant geographic population structure were found among the samples located north of the River Nanliujiang. Based on the reproductive biology of mitten crabs and the geography of their habitat we argue that both natural and human-mediated gene flow are unlikely to fully account for the similar allele frequency distributions at microsatellite loci. Large population sizes of mitten crabs suggest instead that a virtual absence of genetic drift and significant homoplasy of microsatellite alleles have contributed to the observed pattern. Furthermore, a coalescent-based maximum likelihood method indicated a more than two-fold lower effective population size of the Southern population compared to the Northern Group and low but significant levels of gene flow between both areas.

References

  1. Amos W, Flint J, Xu X (2008) Heterozygosity increases microsatellite mutation rate, linking it to demographic history. BMC Genet 9:72PubMedCrossRefGoogle Scholar
  2. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  3. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568. doi:10.1073/pnas.081068098 PubMedCrossRefGoogle Scholar
  4. Carlton JT (1985) Transoceanic and interoceanic dispersal of costal marine organisms, the biology of ballast water. Oceanogr Mar Biol Ann Rev 23:313–371Google Scholar
  5. Cohen AN, Carlton JT (1997) Transoceanic transport mechanisms: introduction of the Chinese mitten crab Eriocheir sinensis, to California. Pac Sci 51:1–11Google Scholar
  6. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedGoogle Scholar
  7. Corander J, Marttinen P, Mantyniemi S (2006) A Bayesian method for identification of stock mixtures from molecular marker data. Fish Bull (Wash DC) 104:550–558Google Scholar
  8. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, LondonGoogle Scholar
  9. Dai AY (1988) A preliminary cladistic analysis on Eriocheir (Crustacea:Decapoda). Acta Zootaxon Sin 13:22–26 (in Chinese with English abstract)Google Scholar
  10. Dai AY (1991) Studies on the subspecies differentiation of the genus Eriocheir (Decapoda:Brachyura). In: Zhang GX (ed) Scientific treatises on systematic and evolutionary zoology, vol 1. China Science and Technology Publication House, Beijing, pp 61–71 (in Chinese with English abstract)Google Scholar
  11. De Meester L, Gomez A, Okamura B, Schwenk K (2002) The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol-Int J Ecol 23:121–135. doi:10.1016/S1146-609X(02)01145-1 CrossRefGoogle Scholar
  12. Doyle JJ, Doyle JL (1985) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  13. Du NS (2004) Migration of Chinese mitten crab. J Fish Sci Technol Info China 31:56–57 in ChineseGoogle Scholar
  14. Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16:551–558. doi:10.1016/S0168-9525(00)02139-9 PubMedCrossRefGoogle Scholar
  15. Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. doi:10.1038/nrg1348 PubMedCrossRefGoogle Scholar
  16. Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604. doi:10.1046/j.1365-294X.2002.01576.x PubMedCrossRefGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  18. FAO (2007) The state of world fisheries and aquaculture 2006. FAO, Rome, p 180Google Scholar
  19. Gao ZQ, Zhou KY (1998) Genetic variation of the Chinese mitten-handed crab (Eriocheir sinensis) populations detected by RAPD analysis. J Biodivers China 6:186–190 (in Chinese with English abstract)Google Scholar
  20. Geyer CJ (1994) Estimating normalizing constants and reweighting mixtures in Markov chain Monte Carlo. Technical Report 568, School of Statistics, University of MinnesotaGoogle Scholar
  21. Geyer CJ, Thompson E (1995) Annealing Markov chain Monte Carlo with applications to ancestral inference. J Am Stat Assoc 90:909–920. doi:10.2307/2291325 CrossRefGoogle Scholar
  22. Goudet J (1995) FSTAT, a program to estimate and test gene diversities and fixation indices (version 1.2). J Hered 86:485–486Google Scholar
  23. Gu XH, Zhao FS (2001) Resources and culturing situation of Chinese mitten crab (Eriocheir sinensis) and species character conversation. J Lake Sci China 13:267–271 (in Chinese with English abstract)Google Scholar
  24. Guo JK, Ng NK, Dai AY, Ng PKL (1997) The taxonomy of three commercially important species of mitten crabs of the genus Eriocheir de Hann, 1835 (Crustacea:Decaposa:Brachyura:Grapsidae). Raffles Bull Zool 45:445–476Google Scholar
  25. Hänfling B (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71:115–135. doi:10.1111/j.1095-8649.2007.01474.x CrossRefGoogle Scholar
  26. Hänfling B, Weetman D (2003) Primer note: characterization of microsatellite loci for the Chinese mitten crab, Eriocheir sinensis. Mol Ecol Notes 3:15–17. doi:10.1046/j.1471-8286.2003.00336.x CrossRefGoogle Scholar
  27. Hänfling B, Weetman D (2006) Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the River Sculpin, Cottus gobio. Genetics 173:1487–1501. doi:10.1534/genetics.105.054296 PubMedCrossRefGoogle Scholar
  28. Hänfling B, Carvalho GR, Brandl R (2002) Note: mt-DNA sequences and possible pathways of the Chinese mitten crab. Mar Ecol Prog Ser 238:307–310. doi:10.3354/meps238307 CrossRefGoogle Scholar
  29. Hauser L, Seamons TR, Dauer M, Naish KA, Quinn TP (2006) An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA. Mol Ecol 15:3157–3173. doi:10.1111/j.1365-294X.2006.03017.x PubMedCrossRefGoogle Scholar
  30. Hedrick PW (1999) Highly variable loci and their interpretations in evolution and conservation. Evol Int J Org Evol 53:313–318. doi:10.2307/2640768 Google Scholar
  31. Herborg LM, Rushton SP, Clare AS, Bentley MG (2003) Spread of the Chinese mitten crab (Eriocheir sinensis H. Milen Edwards) in continental Europe: analysis of a historical data set. Hydrobiologia 503:21–28. doi:10.1023/B:HYDR.0000008483.63314.3c CrossRefGoogle Scholar
  32. Herborg LM, Weetman D, Van Oosterhout C, Hänfling B (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242. doi:10.1111/j.1365-294X.2006.03133.x PubMedCrossRefGoogle Scholar
  33. Hutchinson WF, Carvalho GR, Rogers SI (2001) Marked genetic structuring in localized spawning populations of cod Gadus morhua in the North Sea and adjoining waters, as revealed by microsatellites. Mar Ecol Prog Ser 223:251–260. doi:10.3354/meps223251 CrossRefGoogle Scholar
  34. Kinnison MT, Bentzen P, Unwin MJ, Quinn TP (2002) Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon. Mol Ecol 11:739–754. doi:10.1046/j.1365-294X.2002.01477.x PubMedCrossRefGoogle Scholar
  35. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (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. doi:10.1007/s10592-005-9098-1 CrossRefGoogle Scholar
  36. Li G, Shen Q, Xu ZX (1993) Morphometric and biochemical genetic variation of the mitten crab, Eriocheir, in southern China. Aquaculture 111:103–115. doi:10.1016/0044-8486(93)90029-X CrossRefGoogle Scholar
  37. Li YS, Li SF, Xu GY, Ling WH (2000) Comparison of growth performance of Chinese mitten crab (Eriocheir sinensis) in pen culture from the Yangtze and Liaohe River systems. J Shanghai Fish Univ 9:189–193 (in Chinese with English abstract)Google Scholar
  38. Liu K, Duan DR, Xu DP, Zhang MY, Shi WG (2007) Studies on current resources and causes of catch fluctuation of brooders of mitten crab in estuary of the Yangtze River. J Lake Sci China 19:212–217 in Chinese with English abstractGoogle Scholar
  39. Mariani S, Hutchinson WF, Hatfield EMC, Ruzzante DE, Simmonds EJ, Dahlgren TG, Andre C, Brigham J, Torstensen E, Carvalho GR (2005) North Sea herring population structure revealed by microsatellite analysis. Mar Ecol Prog Ser 303:245–257. doi:10.3354/meps303245 CrossRefGoogle Scholar
  40. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405. doi:10.1034/j.1600-0706.2003.12010.x CrossRefGoogle Scholar
  41. Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, Macisaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035. doi:10.1111/j.1365-294X.2008.03669.x PubMedCrossRefGoogle Scholar
  42. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  43. Pujolar JM, Maes GE, Volckaert FAM (2006) Genetic patchiness among recruits in the European eel Anguilla anguilla. Mar Ecol Prog Ser 307:209–217. doi:10.3354/meps307209 CrossRefGoogle Scholar
  44. Qiu GF (1998) A review of genetics and breeding in shrimps (prawns) and crabs. J Fish China 22:265–274 (in Chinese with English abstract)Google Scholar
  45. Raymond M, Rousset F (1995) GENEPOP-population genetics software for exact tests and ecumenicism (1.2 version). J Hered 86:248–249Google Scholar
  46. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evol Int J Org Evol 55:1095–1103Google Scholar
  47. Rice WR (1989) Analyzing tables of statistical tests. Evol Int J Org Evol 43:223–225. doi:10.2307/2409177 Google Scholar
  48. Rudnick DA, Hieb K, Grimmer KF, Resh VH (2003) Patterns and processes of biological invasion: the Chinese mitten crab in San Francisco Bay. Basic Appl Ecol 4:249–262. doi:10.1078/1439-1791-00152 CrossRefGoogle Scholar
  49. Ruiz GM, Fegley L, Fofonoff P, Cheng YX, Lemaitre R (2006) First records of Eriocheir sinensis H. Milne-Edwards, 1853 (Crustacean:Brachyura:Varunidae) for Chesapeake Bay and the mid-Atlantic coast of North America. Aquat Invas 1:137–142. doi:10.3391/ai.2006.1.3.7 CrossRefGoogle Scholar
  50. Tang BP, Zhou KY, Song DX, Yang G, Dai AY (2003) Molecular systematic of the Asian mitten crabs, genus Eriocheir (Crustacea:Brachyura). Mol Phylogenet Evol 29:309–316. doi:10.1016/S1055-7903(03)00112-X PubMedCrossRefGoogle Scholar
  51. Valle-Jimenez R, Cruz P, Perez-Enriquez R (2005) Population genetic structure of Pacific White Shrimp (Litopenaeus vannamei) from Mexico to Panama: microsatellite DNA variation. Mar Biotechnol 6:475–484. doi:10.1007/s10126-004-3138-6 CrossRefGoogle Scholar
  52. 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. doi:10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  53. Wang CH, Li SF (2002) Advances in studies on germplasm in Chinese mitten crab, Eriocheir sinensis. J Fish China 9:82–86 (in Chinese with English abstract)Google Scholar
  54. Wang D, Yu W (1995) A comparative study on the isozymes in Eriocheir sinensis from Yangtze and Liaohe River. J Liaoning Univ China 22:79–81 (Nature science edition)Google Scholar
  55. Wang CH, Li CH, Li SF (2008) Mitochondrial DNA-inferred population structure and demographic history of the mitten crab (Eriocheir sensu stricto) found along the coast of mainland China. Mol Ecol 17:3515–3527PubMedGoogle Scholar
  56. Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420:191–201. doi:10.1023/A:1003928327503 CrossRefGoogle Scholar
  57. Weetman D, Hauser L, Bayes M, Ellis JR, Shaw PW (2006a) Genetic population structure across a range of geographic scales in the commercial exploited marine gastropod Buccinum undatum. Mar Ecol Prog Ser 317:157–169. doi:10.3354/meps317157 CrossRefGoogle Scholar
  58. Weetman D, Hauser L, Carvalho GR (2006b) Heterogeneous evolution of microsatellites revealed by reconstruction of recent mutation history in an invasive apomictic snail, Potamopyrgus antipodarums. Genetica 127:285–293. doi:10.1007/s10709-005-4847-0 PubMedCrossRefGoogle Scholar
  59. Weir BS, Cockerham CC (1984) Estimating F statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641 Google Scholar
  60. Wirth T, Bernatchez L (2001) Genetic evidence against panmixia in the European eel. Nature 409:1037–1040. doi:10.1038/35059079 PubMedCrossRefGoogle Scholar
  61. Yu LF, Li CS, Chen WZ, Dai GL, Gong ZG, Shi DL (1999) Absence and distribution of Eriocheir sinensis larvae in the mouth of Yangtze River and its preservation strategy. J Fish China 23(suppl):34–38 (in Chinese with English abstract)Google Scholar
  62. Zhang LS, Li J (2002) Larval breeding technology of Eriocheir sinensis. In: Zhang LS (ed) The breeding and culture of Chinese mitten crab. Jingdun Press, Beijing, pp 124–196 (in Chinese)Google Scholar
  63. Zhang LS, Zhai JJ, Wang DD (2000) Ecological and morphological differentiation and identification of Chinese mitten crab Eriocheir sinensis populations from Yangtze, Ou and Liaohe river systems. J Fish Sci Technol Info China 27:200–205 (in Chinese with English abstract)Google Scholar
  64. Zhang LS, Zhu XC, Yuan SQ, Zhu CL, Zhang GX, Li G, Zhang GH, Lu J (2002) Study on forecast of fishing season of Chinese mitten-handed crab (Eriocheir sinensis) seeds at the mouth of Yangtze River. J Fish Sci Technol Info China 29:56–60 (in Chinese with English abstract)Google Scholar
  65. Zhao NG (1980) Experiments on the artificial propagation of the woolly-handed crab (Eriocheir sinensis H. Milne-Edwards) in artificial sea water. J Fish China 4:95–104 (in Chinese with English abstract)Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Liying Sui
    • 1
    • 2
  • Fumin Zhang
    • 3
  • Xiaomei Wang
    • 4
  • Peter Bossier
    • 2
  • Patrick Sorgeloos
    • 2
  • Bernd Hänfling
    • 5
  1. 1.Key Laboratory of Marine Resources and Chemistry of Tianjin, College of Marine Science and EngineeringTianjin University of Science and TechnologyTianjinChina
  2. 2.Laboratory of Aquaculture and Artemia Reference CenterGhent UniversityGhentBelgium
  3. 3.State Key Laboratory of Systematic and Evolutionary BotanyInstitute of Botany, The Chinese Academy of SciencesBeijingChina
  4. 4.Key Laboratory of Aqua-Ecology and AquacultureTianjin Agricultural UniversityTianjinChina
  5. 5.Department of Biological SciencesUniversity of HullHullUK

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