Marine Biology

, 165:9 | Cite as

Comparative population genetic study of an important marine parasite from New Zealand flat oysters

  • Henry S. Lane
  • Brian Jones
  • Robert Poulin
Original paper


The comparative genetic structure of hosts and parasites can reveal constraints acting on parasite dispersal among host populations and the evolution of local adaptation. We sampled New Zealand flat oysters Ostrea chilensis from 12 sites throughout New Zealand to (1) determine the distribution and prevalence of the haplosporidian parasites Bonamia exitiosa and B. ostreae, and (2) test for congruent patterns of host and parasite genetic structure. B. exitiosa was detected at three sites: Hauraki Gulf (5% prevalence), Marlborough Sounds (30%), and Foveaux Strait (7%), whereas B. ostreae was only detected in the Marlborough Sounds (37%). Using nuclear internal transcribed spacer (ITS) rDNA sequences of B. exitiosa, as well as mitochondrial cytochrome c oxidase subunit 1 gene (CO1) sequences of O. chilensis from the same sites plus other key O. chilensis growing areas (Tasman Bay and Chatham Islands), we compared the genetic structure of host and parasite. B. exitiosa displayed genetic structure across all three sites which were reflected in populations of O. chilensis except for gene flow between Tasman Bay-Marlborough Sounds-Chatham Islands. The observed patterns reflect the host specificity of Bonamia parasites and the limited dispersal capability of oysters. O. chilensis may experience long distance dispersal which is likely influenced by oceanographic factors. Nonetheless, a failure to detect Bonamia parasites among genetically connected O. chilensis populations suggests natural long distance co-dispersal of Bonamia parasites with O. chilensis is unlikely. Instead, the dispersal of Bonamia parasites is likely influenced by anthropogenic factors.



We thank New Zealand’s Ministry for Primary Industries (MPI), NIWA, and Kono Seafoods for the efforts in sample collection. The Animal Health Laboratory, Wallaceville, (MPI) provided laboratory resources during the course of this study which was carried out as part of a Ph.D. project at the University of Otago, within Prof. Robert Poulin’s laboratory group. Finally, we thank the anonymous reviewers, whose input greatly improved this manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Abbott CL, Gilmore SR, Lowe G, Meyer G, Bower S (2011) Sequence homogeneity of the internal transcribed spacer rDNA in Mikrocytos mackini and detection of Mikrocytos sp. in a new location. Dis Aquat Org 93:243–250CrossRefGoogle Scholar
  2. Arzul I, Carnegie RB (2015) New perspective on the haplosporidian parasites of molluscs. J Invert Pathol 131:32–42CrossRefGoogle Scholar
  3. Arzul I, Gagnaire B, Bond C et al (2009) Effects of temperature and salinity on the survival of Bonamia ostreae a parasite infecting flat oysters Ostrea edulis. Dis Aquat Org 85:67–75CrossRefGoogle Scholar
  4. Arzul I, Langlade A, Chollet B et al (2011) Can the protozoan parasite Bonamia ostreae infect larvae of flat oysters Ostrea edulis? Vet Parasitol 179:69–76CrossRefGoogle Scholar
  5. Audemard C, Carnegie RB, Stokes NA et al (2008) Effects of salinity on Bonamia sp. survival in Asia oyster Crassostrea ariakensis. J Shell Res 27:535–540CrossRefGoogle Scholar
  6. Audemard C, Carnegie RB, Hill KM, Peterson CH, Burreson EM (2014) Bonamia exitiosa transmission among, and incidence in, Asian oyster Crassostrea ariakensis under warm euhaline conditions. Dis Aquat Org 110:143–150CrossRefGoogle Scholar
  7. Beerli P (2006) Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics 22:341–345CrossRefGoogle Scholar
  8. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci 98:4563–4568CrossRefGoogle Scholar
  9. Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140:1316–1322CrossRefGoogle Scholar
  10. Blasco-Costa I, Waters JM, Poulin R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Mol Ecol 21:207–217CrossRefGoogle Scholar
  11. Broekhuizen N, Lundquist CJ, Hadfield MG, Brown SN (2011) Dispersal of oyster (Ostrea chilensis) larvae in the Tasman Bay inferred using a verified particle tracking model that incorporates larval behaviour. J Shell Res 30:643–658CrossRefGoogle Scholar
  12. Brown GD, Hudson KL, Reece KS (2004) Multiple polymorphic sites at the ITS and ATAN loci in cultured isolates of Perkinsus marinus. J Eukaryot Microbiol 51:312–320CrossRefGoogle Scholar
  13. Bryan SE, Cook AG, Evans JP et al (2012) Rapid, long-distance dispersal by pumice rafting. PLoS One 7:e40583. CrossRefGoogle Scholar
  14. Buroker NE, Chanley P, Cranfield HJ, Dinamani P (1983) Systematic status of two oyster populations of the genus Tiostrea from New Zealand and Chile. Mar Biol 77:191–200CrossRefGoogle Scholar
  15. Bushek D, Ford SE, Burt I (2012) Long-term patterns of an estuarine pathogen along a salinity gradient. J Mar Res 70:225–251CrossRefGoogle Scholar
  16. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  17. Cranfield HJ, Dunn A, Doonan IJ, Michael KP (2005) Bonamia exitiosa epizootic in Ostrea chilensis from Foveaux Strait, southern New Zealand between 1986 and 1992. ICES J Mar Sci 62:3–13CrossRefGoogle Scholar
  18. Criscione CD, Blouin MS (2007) Parasite phylogeographical congruence with salmon host evolutionarily significant units: implications for salmon conservation. Mol Ecol 16:993–1005CrossRefGoogle Scholar
  19. Diggles BK, Hine PM (2002) Bonamia exitiosus epidemiology in Foveaux Strait oysters. National Institute of Water and Atmospheric Research, 2002. Ministry of Fisheries Research Project OYS1999/01AGoogle Scholar
  20. DiSalvo LH, Alarcon E, Martinez E (1983) Induced spat production from Ostrea chilensis Philippi 1845 in mid-winter. Aquaculture 30:357–362CrossRefGoogle Scholar
  21. Engelsma MY, Culloty SC, Lynch SA et al (2014) Bonamia parasites: a rapidly changing perspective on a genus of important mollusc pathogens. Dis Aquat Org 110:5–23CrossRefGoogle Scholar
  22. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefGoogle Scholar
  23. Faurby S, Barber DH (2012) Theoretical limits to the correlation between pelagic larval duration and population genetic structure. Mol Ecol 21:3419–3432CrossRefGoogle Scholar
  24. Feis ME, Thieltges DW, Olsen JL et al (2015) The most vagile host as the main determinant of population connectivity in marine macroparasites. Mar Ecol Prog Ser 520:85–99CrossRefGoogle Scholar
  25. Flannery G (2014) Aspects of the biology of the parasite Bonamia ostreae with a view to gaining a greater understanding of how to alleviate its impact on the European flat oyster, Ostrea edulis. Dissertation, University College Cork, CorkGoogle Scholar
  26. Flannery G, Lynch SA, Culloty SC (2016) Investigating the significance of the role of Ostrea edulis larvae in the transmission and transfer Bonamia ostreae. J Invert Pathol 136:7–9CrossRefGoogle Scholar
  27. Foighil DO, Marshall BA, Hilbish TJ, Pino MA (1999) Trans-Pacific range extension by rafting inferred for the flat oyster Ostrea chilensis. Biol Bull 196:122–126CrossRefGoogle Scholar
  28. Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc Lond 278:649–655CrossRefGoogle Scholar
  29. Haskin HH, Ford SE (1982) Haplosporidium nelsoni (MSX) on Delaware Bay seed oyster beds: a host–parasite relationship along a salinity gradient. J Invert Pathol 40:388–405CrossRefGoogle Scholar
  30. Heath RA (1985) A review of the physical oceanography of the sea around New Zealand—1982. N Z J Mar Fresh Res 19:79–124CrossRefGoogle Scholar
  31. Hill KM, Stokes NA, Webb SC et al (2014) Phylogenetics of Bonamia parasites based on small subunit and internal transcribed spacer region ribosomal DNA sequence data. Dis Aquat Org 110:33–54CrossRefGoogle Scholar
  32. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–446CrossRefGoogle Scholar
  33. Hill-Spanik KM, McDowell JR, Stokes NA et al (2015) Phylogeographic perspective on the distribution and dispersal of a marine pathogen, the oyster parasite Bonamia exitiosa. Mar Ecol Prog Ser 536:65–76CrossRefGoogle Scholar
  34. Hine PM (1991) The annual pattern of infection by Bonamia sp. in New Zealand flat oysters, Tiostrea chilensis. Aquaculture 93:241–251CrossRefGoogle Scholar
  35. Hine PM (1997) Health status of commercially important molluscs in New Zealand. Surveillance 24:25–28Google Scholar
  36. Hine PM, Jones JB (1994) Bonamia and other aquatic parasites of importance to New Zealand. N Z J Zool 21:49–56CrossRefGoogle Scholar
  37. Jeffs AG, Creese RG (1996) Overview and bibliography of research on the Chilean oyster Tiostrea chilensis (Philippi, 1845) from New Zealand waters. J Shell Res 15:305–311Google Scholar
  38. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefGoogle Scholar
  39. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier trasnform. Nucleic Acids Res 30:3059–33066CrossRefGoogle Scholar
  40. Keeney DB, King TM, Rowe DL, Poulin R (2009) Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Mol Ecol 18:4591–4603CrossRefGoogle Scholar
  41. Kroeck MA, Montes J (2005) Occurence of the haemocyte parasite Bonamia sp. in flat oysters Ostrea puelchana farmed in San Antonio Bay (Argentina). Dis Aquat Org 20:231–235CrossRefGoogle Scholar
  42. Lane HS (2017) Studies on Bonamia parasites (Haplosporidia) in the New Zealand flat oyster Ostrea chilensis. Unpublished Dissertation, University of Otago, DunedinGoogle Scholar
  43. Lane HS, Webb SC, Duncan J (2016) Bonamia ostreae in the New Zealand oyster Ostrea chilensis: a new host and geographic record for this haplosporidian parasite. Dis Aquat Org 118:55–63CrossRefGoogle Scholar
  44. Lopez-Flores I, Suarez-Santiago VN, Longet D et al (2007) Characterization of actin genes in Bonamia ostreae and their application to phylogeny of the Haplosporidia. Parasitology 134:1941–1948CrossRefGoogle Scholar
  45. Lynch SA, Armitage DV, Mulcahy MF, Culloty SC (2007) Investigating the possible role of benthic macroinvertebrates and zooplankton in the life cycle of the haplosporidian Bonamia ostreae. Exp Parasitol 115:359–368CrossRefGoogle Scholar
  46. Lynch SA, Abolle E, Ramilo A et al (2010) Observations raise the question if the Pacific Oyster, Crassostrea gigas, can act as either a carrier or reservoir for Bonamia ostreae and Bonamia ostreae. Parasitology 137:1515–1526CrossRefGoogle Scholar
  47. Mazé-Guilmo E, Blanchet S, McCoy KD, Loot G (2016) Host dispersal as the driver of parasite genetic structure: a paradigm lost? Ecol Lett 19:336–347CrossRefGoogle Scholar
  48. Michael KP, Fu D, Forman J, Hulston D (2013) The Foveaux Strait oyster (Ostrea chilensis, OYU5) stock assessment survey and status of Bonamia infection and mortality, February 2012. New Zealand Fisheries Assessment Report 2013/09Google Scholar
  49. Michael KP, Forman J, Hulston D (2015) A survey of the Foveaux Strait oyster (Ostrea chilensis) population (OYU5) commercial fishery areas and the status of Bonamia (Bonamia exitiosa) in February 2015. New Zealand Fisheries Assessment Report 2015/73, p 88Google Scholar
  50. Montes J, Anadón R, Azevedo C (1994) A possible lifecycle for Bonamia ostreae on the basis of electron microscopy studies. J Invert Pathol 53:1–6CrossRefGoogle Scholar
  51. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  52. Prado-Alvarez M, Chollet B, Couraleau Y et al (2013) Heat shock protein 90 of Bonamia ostreae: characterization and possible correlation with infection of the flat oyster, Ostrea edulus. J Eukaryot Microbiol 60:257–266CrossRefGoogle Scholar
  53. Prado-Alvarez M, Couraleau Y, Chollet B et al (2015) Whole-genome amplification: a useful approach to characterize new genes in unculturable protozoan parasites such as Bonamia exitiosa. Parasitology 142:1523–1534CrossRefGoogle Scholar
  54. Ramilo A, Ignacio Navas J, Villalba A, Abollo E (2013) Species-specific diagnostic assays for Bonamia ostreae and B. exitiosa in the European flat oyster Ostrea edulis: conventional, real-time and multiplex PCR. Dis Aquat Org 104:149–161CrossRefGoogle Scholar
  55. Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system ( Mol Ecol Notes 7:355–364CrossRefGoogle Scholar
  56. Ross PM, Hogg ID, Pilditch CA, Lundquist CJ (2009) Phylogeography of New Zealand’s coastal benthos. N Z J Mar Fresh Res 43:1009–1027CrossRefGoogle Scholar
  57. Ross PM, Hogg ID, Pilditch CA et al (2012) Population genetic structure of the New Zealand estuarine clam Austrovenus stutchburyi (Bivalve: Veneridae) reveals populations subdivision and partial congruence with biogeographic boundaries. Estuar Coasts 35:143. CrossRefGoogle Scholar
  58. Santos AM, Cabezas MP, Tavares AI et al (2015) tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics. Google Scholar
  59. Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385CrossRefGoogle Scholar
  60. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  61. Thomas LJ (2015) A molecular and population genetics study of the Bluff oyster (Ostrea chilensis). Dissertation, Victoria University of Wellington, WellingtonGoogle Scholar
  62. Van Banning P (1987) Further results of the Bonamia ostreae challenge tests in Dutch oyster culture. Aquaculture 67:191–194CrossRefGoogle Scholar
  63. Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Ministry for Primary Industries, Animal Health LaboratoryInvestigation and Diagnostic CentreUpper HuttNew Zealand

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