Marine Biotechnology

, Volume 13, Issue 2, pp 181–192 | Cite as

Evolutionary Patterns in Pearl Oysters of the Genus Pinctada (Bivalvia: Pteriidae)

  • Regina L. Cunha
  • Françoise Blanc
  • François Bonhomme
  • Sophie Arnaud-Haond
Original Article


Pearl oysters belonging to the genus Pinctada (Bivalvia: Pteriidae) are widely distributed between the Indo-Pacific and western Atlantic. The existence of both widely distributed and more restricted species makes this group a suitable model to study diversification patterns and prevailing modes of speciation. Phylogenies of eight out of the 11 currently recognised Pinctada species using mitochondrial (cox1) and nuclear (18S rRNA) data yielded two monophyletic groups that correspond to shell size and presence/absence of hinge teeth. Character trace of these morphological characters onto the molecular phylogeny revealed a strong correlation. Pinctada margaritifera appears polyphyletic with specimens from Mauritius grouping in a different clade from others of the French Polynesia and Japan. Hence, P. margaritifera might represent a species complex, and specimens from Mauritius could represent a different species. Regarding the putative species complex Pinctada fucata/Pinctada martensii/Pinctada radiata/Pinctada imbricata, our molecular analyses question the taxonomic validity of the morphological characters used to discriminate P. fucata and P. martensii that exhibited the lowest genetic divergence and are most likely conspecific as they clustered together. P. radiata and P. imbricata were recovered as monophyletic. The absence of overlapping distributions between sister lineages and the observed isolation by distance suggests that allopatry is the prevailing speciation mode in Pinctada. Bayesian dating analysis indicated a Miocene origin for the genus, which is consistent with the fossil record. The northward movement of the Australian plate throughout the Miocene played an important role in the diversification process within Pinctada.


Pinctada Evolutionary patterns Species complex Allopatry Biogeography 



We thank Rita Castilho for helpful discussions and for drawing Figs. 1, 3 and 4. We are very grateful to Annie Orth for maintaining collections in liquid nitrogen for ages and to Christelle Campanini for sequencing P. fucata (GenBank accession number GQ355871).


  1. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Csaksi BNPAF (ed) 2nd International Symposium on Information Theory. Budapest, Hungary, Akademiai KiadoGoogle Scholar
  2. Allan J (1959) Australian shells with related animals living in the sea, in freshwater and on the land. Charles T. Brandford Company, BostonGoogle Scholar
  3. Arbogast BS, Slowinski JB (1998) Pleistocene speciation and the mitochondrial DNA clock. Science 282:1955CrossRefGoogle Scholar
  4. Arnaud-Haond S, Vonau V, Bonhomme F, Boudry P, Prou J, Seaman T (2003a) Sustainable management of local genetic resources of the pearl oyster (Pinctada margaritifera cumingii) in French Polynesia: an evaluation of the potential impact of the cultural practice of spat collection. Aquaculture 219:181–192CrossRefGoogle Scholar
  5. Arnaud-Haond S, Monteforte M, Blanc F, Bonhomme F (2003b) Evidence for male-biased effective sex ratio and recent step-by-step colonization in the bivalve Pinctada mazatlanica. J Evol Biol 16:790–796PubMedCrossRefGoogle Scholar
  6. Arnaud-Haond S, Bonhomme F, Blanc F (2003c) Large discrepancies in differentiation of allozymes, nuclear and mitochondrial DNA loci in recently founded Pacific populations of the pearl oyster Pinctada margaritifera. J Evol Biol 16:388–398PubMedCrossRefGoogle Scholar
  7. Arnaud-Haond S, Monteforte M, Bonhomme F, Blanc F (2000) Population structure and genetic variability of pearl oyster. Pinctada mazatlanica along Pacific coasts from Mexico to Panama Conservation Genetics 1:299–307Google Scholar
  8. Arnaud-Haond S, Vonau V, Boudry P, Blanc F, Prou J, Seaman T, Goyard E (2004) Spatio-temporal variation in the genetic composition of wild populations of pearl oyster (Pinctada margaritifera cumingii) in French Polynesia following 10 years of juvenile translocation. Mol Ecol 13:2001–2007PubMedCrossRefGoogle Scholar
  9. Arnaud-Haond S, Vonau V, Rouxel C, Bonhomme F, Prou J, Goyard E, Boudry P (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Mar Biol 155:147–157CrossRefGoogle Scholar
  10. Benzie JA, Smith-Keune C (2006) Microsatellite variation in Australian and Indonesian pearl oyster Pinctada maxima populations. Mar Ecol Prog Ser 314:197–211CrossRefGoogle Scholar
  11. Bondad-Reantaso MG, McGladdery SE, Berthe FCJ (2007) Pearl oyster health management - a manual. FAO Fisheries Technical Paper. Food and agriculture organization of the United Nations, RomeGoogle Scholar
  12. Caretto PG (1975) Un raro lamellibranco perlifero nel Pliocene Piemontese. Atti Soc ital sci nat mus civ stor nat Milano 116:33–64Google Scholar
  13. Caretto PG, Durand P, Blanc F (1989) Apport de l'analyse biométrique à l'étude des relations phylogénétiques de la nacre fossile Pteria margaritifera studeri (Mayer) (Mollusque, bivalve, Pteriidae). Atti Soc ital sci nat mus civ stor nat Milano 130:205–216Google Scholar
  14. Drummond AJ, Ho SYW, Philips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88PubMedCrossRefGoogle Scholar
  15. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  16. Frey MA, Vermeij GJ (2008) Molecular phylogenies and historical biogeography of a circumtropical group of gastropods (Genus: Nerita): implications for regional diversity patterns in the marine tropics. Mol Phylogenet Evol 48:1067–1086PubMedCrossRefGoogle Scholar
  17. Gervis MH, Sims NA (1992) The biology and culture of pearl oysters (Bivalvia: Pteriidae). The WorldFish Center, LondonGoogle Scholar
  18. Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  19. Hertlein LG, Cox LR (1969) Family Pteriidae Gray, 1847 (1820). In: Cox LR, Newell ND, Boyd DW, Branson CC, Casey R, Chavan R, Coogan AH, Dechaseaux AH, Fleming C, Haas CA, Hertlein F, Kauffman LG, Keen EG, Larocque AM, McAlester AL, Moore AL, Nuttal RC, Perkins BF, Puri HS, Smith LA, Soot-Ryen T, Stenzel HB, Trueman ER, Turner RD, Weir J (eds) Treatise on invertebrate paleontology, Part N. Mollusca 6: Bivalvia, vol 1. Geological Society of America and University of Kansas, LawrenceGoogle Scholar
  20. Hodell DA, Vayavananda A (1993) Middle Miocene paleooceanography of the western equatorial Pacific (DSDP site 289) and the evolution of Globorotalia (Fohsella). Mar Micropaleontol 22:279–310CrossRefGoogle Scholar
  21. Hollander J (2008) Testing the grain-size model for the evolution of phenotypic plasticity. Evolution 62:1381–1389PubMedCrossRefGoogle Scholar
  22. Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  23. Hynd JS (1955) A revision of the Australian pearl-shells, genus Pinctada (Lamellibranchia). Aust J Mar Freshw Res 6:98–137CrossRefGoogle Scholar
  24. Jameson HL (1901) On the identity and distribution of the mother-of-pearl oysters; with a revision of the sub-genus Margaritifera. Proceedings of the General Meetings for Scientific Business of the Zoological Society of London 1:372–394Google Scholar
  25. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975PubMedCrossRefGoogle Scholar
  26. Maddison WP, Maddison DR (2001) MacClade 4 version 4.03PPC. In: Associates S (ed) Sunderlan d, MassachussetsGoogle Scholar
  27. Masaoka T, Kobayashi T (2005) Natural hybridization between Pinctada fucata and Pinctada maculata inferred from internal transcribed spacer regions of nuclear ribosomal RNA genes. Fish Sci 71:829–836CrossRefGoogle Scholar
  28. McCafferty S, Bermingham E, Quenouille B, Planes S, Hoelzer G, Asoh K (2002) Historical biogeography and molecular systematics of the Indo-Pacific genus Dascyllus (Teleostei: Pomacentridae). Mol Ecol 11:1377–1392PubMedCrossRefGoogle Scholar
  29. McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400PubMedCrossRefGoogle Scholar
  30. Meyer CP (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biol J Linn Soc 79:401–459CrossRefGoogle Scholar
  31. Moore EJ (1983) Tertiary marine pelecypods of California and Baja California: Nuculidae through Malleidae. Geol Surv Prof Pap 1228:1–108Google Scholar
  32. Moore WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726CrossRefGoogle Scholar
  33. Oliver PG (1992) Bivalved seashells of the Red Sea. Hemmen and National Museum of Wales, WiesbadenGoogle Scholar
  34. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Ann Rev of Ecolog Syst 25:547–572CrossRefGoogle Scholar
  35. Paulay G, Meyer C (2002) Diversification in the tropical pacific: comparisons between marine and terrestrial systems and the importance of founder speciation. Integr Comp Biol 42:922–934CrossRefGoogle Scholar
  36. Paulay G, Meyer C (2006) Dispersal and divergence across the greatest ocean region: do larvae matter? Integr Comp Biol 46:269–281CrossRefGoogle Scholar
  37. Posada D, Crandall ED (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  38. Radtkey RR, Fallon SM, Case TJ (1997) Character displacement in some Cnemidophorus lizards revisited: a phylogenetic analysis. Proc Natl Acad Sci 94:9740–9745PubMedCrossRefGoogle Scholar
  39. Rambaut A, Drummond AJ (2007) Tracer version 1.4. In: (Ed)
  40. Ranson G (1961) Les especes d'huitres perliéres du genre Pinctada (biologie de quelques-unes d'entre elles). In: Belgique, IRDSND (ed) Mémoires, deuxieme serie, fas, 67Google Scholar
  41. Rüber L, van Tassell JL, Zardoya R (2003) Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 57:1584–1598PubMedGoogle Scholar
  42. Rutschmann F, Erkisson T, Asalim KA, Conti E (2007) Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points. Syst Biol 56:591–608PubMedCrossRefGoogle Scholar
  43. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor laboratory, New YorkGoogle Scholar
  44. Skelton PW, Benton MJ (1993) Mollusca: Rostroconchia, Scaphopoda and Bivalvia. In: Benton MJ (ed) The fossil record2. Chapman & Hall, LondonGoogle Scholar
  45. Sota T, Vogler AP (2001) Incongruence of mitochondrial and nuclear gene trees in the Carabid beetles Ohomopterus. Syst Biol 50:39–59PubMedGoogle Scholar
  46. Southgate PC (2007) Overview of the cultured marine pearl industry. In: Bondad-Reantaso MG, McGladdery SE, Berthe FCJ (eds) Pearl oyster health management: a manual. FAO, RomeGoogle Scholar
  47. Strack E (2008) Introduction. In: Southgate PC, Lucas JS (eds) The pearl oyster. Elsevier, The NetherlandsGoogle Scholar
  48. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109PubMedCrossRefGoogle Scholar
  49. Tëmkin I (2006) Morphological perspective on the classification and evolution of recent Pterioidea (Mollusca: Bivalvia). Zool J Linn Soc 148:253–312CrossRefGoogle Scholar
  50. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin J, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  51. Vermeij GJ (1987) The dispersal barrier in the tropical pacific: implications for molluscan speciation and extinction. Evolution 41:1046–1058CrossRefGoogle Scholar
  52. Wada KT, Tëmkin I (2008) Taxonomy and phylogeny. In: Southgate PC, Lucas JS (eds) The pearl oyster. Elsevier, The NetherlandsGoogle Scholar
  53. Wahlberg N, Braby MF, Brower AVZ, Jong R, Lee M, Nylin S, Pierce NE, Sperling FAH, Vila R, Warren AD, Evgueni (2005) Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers. Proc R Soc Lond B Biol Sci 272:1577–1586CrossRefGoogle Scholar
  54. Wang H, Guo X, Zhang G, Zhanga F (2004) Classification of jinjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquaculture 242:137–155CrossRefGoogle Scholar
  55. Williams ST, Reid DG (2004) Speciation and diversity on tropical rocky shores: a global phylogeny of snails of the genus Echinolittorina. Evolution 58:2227–2251PubMedGoogle Scholar
  56. Yu DH, Chu KH (2006) Species identity and phylogenetic relationship of the pearl oysters in Pinctada Röding, 1798 based on ITS sequence analysis. Biochem Syst Ecol 34:240–250CrossRefGoogle Scholar
  57. Yu DH, Jia X, Chu KH (2006) Common pearl oysters in China, Japan, and Australia are conspecific: evidence from ITS sequences and AFLP. Fish Sci 72:1183–1190CrossRefGoogle Scholar
  58. Yule GU (1924) A mathematical theory of evolution, based on the conclusions of Dr. J. C. Willis. Philos Trans R Soc Lond b 213:21–87CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Regina L. Cunha
    • 1
  • Françoise Blanc
    • 3
  • François Bonhomme
    • 2
  • Sophie Arnaud-Haond
    • 2
    • 4
  1. 1.CCMarUniversidade do AlgarveFaroPortugal
  2. 2.Laboratoire de ZoogéographieUniversité Montpellier IIIMontpellier Cedex 5France
  3. 3.Laboratoire “Génome, Populations, Interactions”Station Méditerranéenne de l’Environnement LittoralSèteFrance
  4. 4.Etude des Ecosystèmes Profonds (DEEP)Centre de Brest de l IFREMERPlouzané CedexFrance

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