Marine Biotechnology

, Volume 18, Issue 2, pp 242–254 | Cite as

Intraspecific Variation in Mitogenomes of Five Crassostrea Species Provides Insight into Oyster Diversification and Speciation

Original Article

Abstract

A large number of Crassostrea oysters are found in Asia-Pacific. While analyses of interspecific variation have helped to establish historical relationships among these species, studies on intraspecific variation are necessary to understand their recent evolutionary history and current forces driving population biology. We resequenced 18 and analyzed 31 mitogenomes of five Crassostrea species from China: Crassostrea gigas, Crassostrea angulata, Crassostrea sikamea, Crassostrea ariakensis, and Crassostrea hongkongensis. Our analysis finds abundant insertions, deletions, and single-nucleotide polymorphisms in all species. Intraspecific variation varies greatly among species with polymorphic sites ranging from 54 to 293 and nucleotide diversity ranging from 0.00106 to 0.00683. In all measurements, C. hongkongensis that has the narrowest geographic distribution exhibits the least sequence diversity; C. ariakensis that has the widest distribution shows the highest diversity, and species with intermediate distribution show intermediate levels of diversity. Low sequence diversity in C. hongkongensis may reflect recent bottlenecks that are probably exacerbated by human transplantation. High diversity in C. ariakensis is likely due to divergence of northern and southern China populations that have been separated without gene flow. The significant differences in mitogenome diversity suggest that the five sister species of Crassostrea have experienced different evolutionary forces since their divergence. The recent divergence of two C. ariakensis populations and the C. gigas/angulata species complex provides evidence for continued diversification and speciation of Crassostrea species along China’s coast, which are shaped by unknown mechanisms in a north–south divide.

Keywords

Mitogenome diversity Crassostrea oyster Phylogeography Population genetics Speciation Evolution 

Supplementary material

10126_2016_9686_MOESM1_ESM.xlsx (249 kb)
ESM 1(XLSX 248 kb)
10126_2016_9686_MOESM2_ESM.docx (1.1 mb)
ESM 2Table S2 (sample information), Table S3 (sequence variation) and Figure S1 (alignment) of a selected mitogenome fragment flanking a 7-bp indel that separates C. ariakensis from north and south China. (DOCX 1.07 mb)

References

  1. Bernard FR, Cai YY, Morton B (1993) Catalogue of living marine bivalve molluscs of China. Hong Kong University Press, Hong KongGoogle Scholar
  2. Bjork A, Liu W, Wertheim JO, Hahn BH, Worobey M (2011) Evolutionary history of chimpanzees inferred from complete mitochondrial genomes. Mol Biol Evol 28:615–623CrossRefPubMedPubMedCentralGoogle Scholar
  3. Carr SM, Marshall HD (2008) Intraspecific phylogeographic genomics from multiple complete mtDNA genomes in Atlantic cod (Gadus morhua): origins of the “codmother,” transatlantic vicariance and midglacial population expansion. Genetics 180:381–389CrossRefPubMedPubMedCentralGoogle Scholar
  4. Danic-Tchaleu G, Heurtebise S, Morga B, Lapegue S (2011) Complete mitochondrial DNA sequence of the European flat oyster Ostrea edulis confirms Ostreidae classification. BMC Res Notes 4:400CrossRefPubMedPubMedCentralGoogle Scholar
  5. Dong C, Xu J, Wang B, Feng J, Jeney Z, Sun X, Xu P (2015) Phylogeny and evolution of multiple common carp (Cyprinus carpio L.) populations clarified by phylogenetic analysis based on complete mitochondrial genomes. Mar Biotechnol 17:565–575CrossRefPubMedGoogle Scholar
  6. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  7. Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194CrossRefPubMedGoogle Scholar
  9. Fridjonsson O, Olafsson K, Tompsett S, Bjornsdottir S, Consuegra S, Knox D, de Leaniz CG, Magnusdottir S, Olafsdottir G, Verspoor E et al (2011) Detection and mapping of mtDNA SNPs in Atlantic salmon using high throughput DNA sequencing. BMC Genomics 12:179CrossRefPubMedPubMedCentralGoogle Scholar
  10. Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202CrossRefPubMedGoogle Scholar
  11. Gordon D, Desmarais C, Green P (2001) Automated finishing with autofinish. Genome Res 11:614–625CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gunnarsdottir ED, Li M, Bauchet M, Finstermeier K, Stoneking M (2011) High-throughput sequencing of complete human mtDNA genomes from the Philippines. Genome Res 21:1–11CrossRefPubMedPubMedCentralGoogle Scholar
  13. Guo X (2009) Use and exchange of genetic resources in molluscan aquaculture. Rev Aquac 1:251–259CrossRefGoogle Scholar
  14. Guo X, Ford S, Zhang F (1999) Molluscan aquaculture in China. J Shellfish Res 18:19–31Google Scholar
  15. Guo X, Zhang G, Qian L, Wang H, Liu X, Wang A (2006) Oysters and oyster farming in china: a review. J Shellfish Res 25:734Google Scholar
  16. Guo X, He Y, Zhang L, Lelong C, Jouaux A (2015) Immune and stress responses in oysters with insights on adaptation. Fish Shellfish Immunol 46:107–119CrossRefPubMedGoogle Scholar
  17. Jacobsen MW, Hansen MM, Orlando L, Bekkevold D, Bernatchez L, Willerslev E, Gilbert MT (2012) Mitogenome sequencing reveals shallow evolutionary histories and recent divergence time between morphologically and ecologically distinct European whitefish (Coregonus spp.). Mol Ecol 21:2727–2742CrossRefPubMedGoogle Scholar
  18. Johansen SD, Coucheron DH, Andreassen M, Karlsen BO, Furmanek T, Jorgensen TE, Emblem A, Breines R, Nordeide JT, Moum T et al (2009) Large-scale sequence analyses of Atlantic cod. N Biotechnol 25:263–271CrossRefPubMedGoogle Scholar
  19. Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304CrossRefPubMedPubMedCentralGoogle Scholar
  20. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  21. Li X, Qi Z (1994) Studies on the comparative anatomy, systematic classification and evolution of Chinese oysters. Stud Mar Sin 35:143–173 (In Chinese)Google Scholar
  22. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  23. Milbury C, Gaffney P (2005) Complete mitochondrial DNA sequence of the Eastern Oyster Crassostrea virginica. Mar Biotechnol 7:697–712CrossRefPubMedGoogle Scholar
  24. Miller PA, Elliott NG, Koutoulis A, Kube PD, Vaillancourt RE (2012) Genetic diversity of cultured, naturalized, and native Pacific oysters, Crassostrea gigas, determined from multiplexed microsatellite markers. J Shellfish Res 31:611–617CrossRefGoogle Scholar
  25. Morin PA, Archer FI, Foote AD, Vilstrup J, Allen EE, Wade P, Durban J, Parsons K, Pitman R, Li L et al (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20:908–916CrossRefPubMedPubMedCentralGoogle Scholar
  26. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  27. Ren J, Liu X, Zhang G, Liu B, Guo X (2009) “Tandem duplication-random loss” is not a real feature of oyster mitochondrial genomes. BMC Genomics 10:84CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ren J, Liu X, Jiang F, Guo X, Liu B (2010a) Unusual conservation of mitochondrial gene order in Crassostrea oysters: evidence for recent speciation in Asia. BMC Evol Biol 10:394CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ren J, Shen X, Jiang F, Liu B (2010b) The mitochondrial genomes of two scallops, Argopecten irradians and Chlamys farreri (Mollusca: Bivalvia): the most highly rearranged gene order in the family Pectinidae. J Mol Evol 70:57–68CrossRefPubMedGoogle Scholar
  30. Roux C, Fraïsse C, Castric V, Vekemans X, Pogson G, Bierne N (2014) Can we continue to neglect genomic variation in introgression rates when inferring the history of speciation? A case study in a Mytilus hybrid zone. J Evol Biol 27:1662–1675CrossRefPubMedGoogle Scholar
  31. Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643–689CrossRefGoogle Scholar
  32. Schonberg A, Theunert C, Li M, Stoneking M, Nasidze I (2011) High-throughput sequencing of complete human mtDNA genomes from the Caucasus and West Asia: high diversity and demographic inferences. Eur J Hum Genet 19:988–994CrossRefPubMedPubMedCentralGoogle Scholar
  33. Stone AC, Battistuzzi FU, Kubatko LS, Perry GH Jr, Trudeau E, Lin H, Kumar S (2010) More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure. Philos Trans R Soc Lond B Biol Sci 365:3277–3288CrossRefPubMedPubMedCentralGoogle Scholar
  34. Teacher AG, Andre C, Merila J, Wheat CW (2012) Whole mitochondrial genome scan for population structure and selection in the Atlantic herring. BMC Evol Biol 12:248CrossRefPubMedPubMedCentralGoogle Scholar
  35. Volatiana JA, Fang S, Kinaro ZO, Liu X (2015) Complete mitochondrial DNA sequences of Saccostrea mordax and Saccostrea cucullata: genome organization and phylogeny analysis. Mitochondrial DNA. 30:1--2Google Scholar
  36. Wang H, Guo X (2008) Identification of Crassostrea ariakensis and related oysters by multiplex species-specific PCR. J Shellfish Res 27:481–487CrossRefGoogle Scholar
  37. Wang H, Guo X, Zhang G, Zhang F (2004) Classification of jinjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquaculture 242:137–155CrossRefGoogle Scholar
  38. Wang H, Zhang G, Liu X, Guo X (2008) Classification of common oysters from North China. J Shellfish Res 27:495–503CrossRefGoogle Scholar
  39. Wang H, Qian L, Liu X, Zhang G, Guo X (2010) Classification of a common cupped oyster from southern China. J Shellfish Res 29:857–866CrossRefGoogle Scholar
  40. Wang H, Qian L, Wang A, Guo X (2013) Occurrence and distribution of Crassostrea sikamea (Amemiya 1928) in China. J Shellfish Res 32:439–446CrossRefGoogle Scholar
  41. Winkelmann I, Campos PF, Strugnell J, Cherel Y, Smith PJ, Kubodera T, Allcock L, Kampmann M-L, Schroeder H, Guerra A et al (2013) Mitochondrial genome diversity and population structure of the giant squid Architeuthis: genetics sheds new light on one of the most enigmatic marine species. Proc R Soc Lond Ser B Biol Sci 280:20130273CrossRefGoogle Scholar
  42. Wu X, Xu X, Yu Z, Wei Z, Xia J (2010) Comparison of seven Crassostrea mitogenomes and phylogenetic analyses. Mol Phylogenet Evol 57:448–454CrossRefPubMedGoogle Scholar
  43. Wu X, Li X, Li L, Xu X, Xia J, Yu Z (2012a) New features of Asian Crassostrea oyster mitochondrial genomes: a novel alloacceptor tRNA gene recruitment and two novel ORFs. Gene 507:112–118CrossRefPubMedGoogle Scholar
  44. Wu X, Li X, Li L, Yu Z (2012b) A unique tRNA gene family and a novel, highly expressed ORF in the mitochondrial genome of the silver-lip pearl oyster, Pinctada maxima (Bivalvia: Pteriidae). Gene 510:22–31CrossRefPubMedGoogle Scholar
  45. Xiao J, Cordes J, Wang H, Guo X, Reece K (2010) Population genetics of Crassostrea ariakensis in Asia inferred from microsatellite markers. Mar Biol 157:1767–1781CrossRefGoogle Scholar
  46. Xiao S, Wu X, Li L, Yu Z (2015) Complete mitochondrial genome of the Olympia oyster Ostrea lurida (Bivalvia, Ostreidae). Mitochondrial DNA 26:471–472CrossRefPubMedGoogle Scholar
  47. Yasuike M, Leong J, Jantzen SG, von Schalburg KR, Nilsen F, Jones SR, Koop BF (2012) Genomic resources for sea lice: analysis of ESTs and mitochondrial genomes. Mar Biotechnol 14:155–166CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yu H, Li Q (2007) Genetic variation of wild and hatchery populations of the Pacific oyster Crassostrea gigas assessed by microsatellite markers. J Genet Genomics 34:1114–1122CrossRefPubMedGoogle Scholar
  49. Yu H, Li Q (2011) Mutation and selection on the wobble nucleotide in tRNA anticodons in marine bivalve mitochondrial genomes. PLoS One 6:e16147CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yu H, Li Q (2012) Complete mitochondrial DNA sequence of Crassostrea nippona: comparative and phylogenomic studies on seven commercial Crassostrea species. Mol Biol Rep 39:999–1009CrossRefPubMedGoogle Scholar
  51. Yu Z, Wei Z, Kong X, Shi W (2008) Complete mitochondrial DNA sequence of oyster Crassostrea hongkongensis—a case of “Tandem duplication-random loss” for genome rearrangement in Crassostrea? BMC Genomics 9:477CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Key Laboratory of Exploration and Utilization of Aquatic Genetic ResourcesShanghai Ocean University, Ministry of EducationShanghaiChina
  2. 2.Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  3. 3.Haskin Shellfish Research Laboratory, Department of Marine and Coastal SciencesRutgers UniversityPort NorrisUSA
  4. 4.Epigenomics and Computational Biology Lab, Virginia Bioinformatics InstituteVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  5. 5.Center of Systematic Genomics, Xinjiang Institute of Ecology and GeographyChinese Academy of SciencesUrumqiChina

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