Marine Biology

, Volume 158, Issue 6, pp 1417–1429 | Cite as

Low to moderate levels of genetic differentiation detected across the distribution of the New Zealand abalone, Haliotis iris

  • Margaret Will
  • Marie L. Hale
  • David R. Schiel
  • Neil J. GemmellEmail author
Original Paper


Two regions of the mitochondrial genome (cytochrome oxidase I and ATPase 8–ATPase 6) were used to examine the population genetic structure of New Zealand’s endemic abalone (Haliotis iris). Samples were collected from 28 locations around New Zealand between January 2005 and February 2008. At least four phylogeographic breaks were present and occurred across the Chatham rise, in the western Cook Strait region, along the southeast coast of the South Island, and at East Cape in the North Island. Gene flow across the Chatham rise is probably limited due to infrequent dispersal across large geographic distances (~850 km), while factors limiting gene flow around the North and South Islands are less clear, and understanding these may require intense temporal and spatial sampling in complex hydrographic regions. High genetic diversity and weak genetic structure may be a general feature of abalone potentially reflecting large and/or ancient populations.


Gene Flow Genetic Structure Mismatch Distribution High Haplotype Diversity Island Sample 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was funded by the New Zealand Ministry of Fisheries Tender GEN2007/A, the Minority International Research Training Program, and the University of Canterbury’s Targeted and Canterbury Scholarships. Amplifications were sequenced at the University of Canterbury Sequencing and Genotyping service. Thanks to the many people and companies who assisted collecting samples (in alphabetical order): Ed Arron, Andy Basset, Paul Buisson, Joe Burke, Burkhart Fisheries Ltd, Ra Clay, Christine Conway, Jeremy Cooper, Department of Conservation, Paul Ferguson, Sharyn Goldstien, Steve Ham, Hal Hovell, Peter Keesing, Ra Kohere, Warrick Lyons, Peter Molloy, Erica Mendietta, Ministry of Fisheries, Riverton Fisheries Ltd, Tammy Steeves, Gerard Prendeville, Top Cat Abalone & Venison Products, and Martin Williams.

Supplementary material

227_2011_1659_MOESM1_ESM.doc (394 kb)
Supplementary material 1 (DOC 393 kb)


  1. Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337CrossRefGoogle Scholar
  2. Apte S, Gardner JPA (2002) Population genetic subdivision in the New Zealand greenshell mussel (Perna canaliculus) inferred from single-strand conformation polymorphism analysis of mitochondrial DNA. Mol Ecol 11:1617–1628CrossRefGoogle Scholar
  3. Ayers KL, Waters JM (2005) Marine biogeographic disjunction in central New Zealand. Mar Biol 147:1045–1052CrossRefGoogle Scholar
  4. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefGoogle Scholar
  5. Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evolution 60:1825–1839CrossRefGoogle Scholar
  6. Barnes EJ (1985) Eastern Cook Strait region circulation inferred from satellite-derived, sea-surface, temperature data. N Z J Mar Freshwater Res 19:405–411CrossRefGoogle Scholar
  7. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefGoogle Scholar
  8. Bowman MJ, Kibblewhite AC, Murtagh RA, Chiswell SM, Sanderson BG (1983) Circulation and mixing in greater Cook Strait, New Zealand. Oceanol Acta 6:383–391Google Scholar
  9. Burton RS, Tegner MJ (2000) Enhancement of red abalone Haliotis rufescens stocks at San Miguel Island: reassessing a success story. Mar Ecol Prog Ser 202:303–308CrossRefGoogle Scholar
  10. Cassens I, Mardulyn P, Milinkovitch MC (2005) Evaluating intraspecific “Network” construction methods using simulated sequence data: do existing algorithms outperform the global maximum parsimony approach? Syst Biol 54:363–372CrossRefGoogle Scholar
  11. Chiswell SM (2009) Colonisation and connectivity by intertidal limpets among New Zealand, Chatham and Sub-Antarctic Islands. II. Oceanographic connections. Mar Ecol Prog Ser 388:121–135CrossRefGoogle Scholar
  12. Chiswell SM, Roemmich D (1998) The East Cape current and two eddies: a mechanism for larval retention? N Z J Mar Freshwater Res 32:385–397CrossRefGoogle Scholar
  13. Clarke CB (2001) Growth and survival of Haliotis iris in northern New Zealand. Dissertation, University of Auckland, Auckland, New ZealandGoogle Scholar
  14. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  15. Conod N, Bartlett JP, Evans BS, Elliott NG (2002) Comparison of mitochondrial and nuclear DNA analyses of population structure in the blacklip abalone Haliotis rubra Leach. Mar Freshw Res 53:711–718CrossRefGoogle Scholar
  16. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefGoogle Scholar
  17. Evans BS, Sweijd NA, Bowie RCK, Cook PA, Elliott NG (2004) Population genetic structure of the perlemoen Haliotis midae in South Africa: evidence of range expansion and founder events. Mar Ecol Prog Ser 270:163–172CrossRefGoogle Scholar
  18. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864CrossRefGoogle Scholar
  19. Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359PubMedPubMedCentralGoogle Scholar
  20. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  21. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  22. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  23. Francis MP (1996) Geographic distribution of marine reef fishes in the New Zealand region. N Z J Mar Freshwater Res 30:35–55CrossRefGoogle Scholar
  24. Frusin A (1982) Electrophoretic study of some paua (Haliotis iris) proteins. Master Thesis, Victoria University, Wellington, New ZealandGoogle Scholar
  25. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedPubMedCentralGoogle Scholar
  26. Gemmell NJ, Akiyama S (1996) An efficient method for the extraction of DNA from vertebrate tissues. Trends Genet 12:338–339CrossRefGoogle Scholar
  27. Goldstien SJ, Schiel DR, Gemmell NJ (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268CrossRefGoogle Scholar
  28. Goldstien SJ, Gemmell NJ, Schiel DR (2009) Colonisation and connectivity by intertidal limpets among New Zealand, Chatham and Sub-Antarctic Islands. I. Genetic connections. Mar Ecol Prog Ser 388:111–119CrossRefGoogle Scholar
  29. Gruenthal KM, Burton RS (2008) Genetic structure of natural populations of the California black abalone (Haliotis cracherodii Leach, 1814), a candidate for endangered species status. J Exp Mar Biol Ecol 355:47–58CrossRefGoogle Scholar
  30. Gruenthal KM, Acheson LK, Burton RS (2007) Genetic structure of natural populations of California red abalone (Haliotis rufescens) using multiple genetic markers. Mar Biol 152:1237–1248CrossRefGoogle Scholar
  31. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefGoogle Scholar
  32. Hara M, Sekino M (2005) Genetic difference between Ezo-awabi Haliotis discus hannai and Kuro-awabi H. discus populations: microsatellite-based population analysis in Japanese abalone. Fish Sci 71:754–766CrossRefGoogle Scholar
  33. Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) The genetic structure of ancient human populations. Curr Anthropol 34:483–496CrossRefGoogle Scholar
  34. Harris TFW (1990) Greater Cook Strait: form and flow. New Zealand Oceanographic Institute: DSIR Marine and Freshwater, Wellington, New ZealandGoogle Scholar
  35. Hauser L, Adcock GJ, Smith PJ, Ramirez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747CrossRefGoogle Scholar
  36. Heath RA (1970) Hydrology and circulation in central and southern Cook Strait, New Zealand. N Z J Mar Freshwater Res 5:178–199CrossRefGoogle Scholar
  37. Heath RA (1972) Oceanic upwelling produced by northerly winds on the north Canterbury coast, New Zealand. N Z J Mar Freshwater Res 6:343–351CrossRefGoogle Scholar
  38. Heath RA (1978) Semidiurnal tides in cook strait. N Z J Mar Freshwater Res 12:87–97CrossRefGoogle Scholar
  39. Heath RA (1985) A review of the physical oceanography of the seas around New Zealand–1982. N Z J Mar Freshwater Res 19:79–124CrossRefGoogle Scholar
  40. Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates. Bull Mar Sci 39:550–564Google Scholar
  41. Hedgecock D (1994) Does variance in reproductive success limit effective population size of marine organisms? In: Beaumont RA (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp 122–134Google Scholar
  42. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290Google Scholar
  43. Holsinger KE, Weir BS (2009) Genetics in geographically structured populations: defining, estimating and interpreting FST. Nature Rev Genet 10:639–650CrossRefGoogle Scholar
  44. Hooker SH, Creese RG (1995) Reproduction of Paua, Haliotis iris Gmelin 1791 (Mollusca, Gastropoda), in north-eastern New Zealand. Mar Freshw Res 46:617–622CrossRefGoogle Scholar
  45. Hume TM, Bell RG, Delange WP, Healy TR, Hicks DM, Kirk RM (1992) Coastal oceanography and sedimentology in New Zealand, 1967–91. N Z J Mar Freshwater Res 26:1–36CrossRefGoogle Scholar
  46. Imron, Jeffrey B, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecol 16:289–304PubMedGoogle Scholar
  47. Kalinowski S (2002) How many alleles per locus should be used to estimate genetic distances? Heredity 88:62–65CrossRefGoogle Scholar
  48. Kalinowski S (2005) Do polymorphic loci require large sample sizes to estimate genetic distances? Heredity 94:33–36CrossRefGoogle Scholar
  49. Laing A, Chiswell S (2003) The ocean medium. In: Andrew N, Francis M (eds) The living reef: the ecology of New Zealand’s rocky reefs. Craig Potton Publishing, Nelson, New Zealand, pp 24–31Google Scholar
  50. Lee HJ, Boulding EG (2007) Mitochondrial DNA variation in space and time in the northeastern Pacific gastropod, Littorina keenae. Mol Ecol 16:3084–3103CrossRefGoogle Scholar
  51. Lee HJ, Boulding EG (2009) Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers. Mol Ecol 18:2165–2184CrossRefGoogle Scholar
  52. Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Vainola R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89:S108–S122CrossRefGoogle Scholar
  53. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190CrossRefGoogle Scholar
  54. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220Google Scholar
  55. Maynard BT, Kerr LJ, McKiernan JM, Jansen ES, Hanna PJ (2005) Mitochondrial DNA sequence and gene organization in Australian backup abalone Haliotis rubra (Leach). Mar Biotechnol 7:645–658CrossRefGoogle Scholar
  56. McShane PE (1992) Early life history of abalone: a review. In: Shepherd SA, Tegner MJ, Guzman Del Proo SA (eds) Abalone of the world: biology, fisheries and culture. Fishing News Books, Oxford, pp 120–138Google Scholar
  57. McShane PE, Naylor JR (1995) Depth can affect postsettlement survival of Haliotis iris (Mollusca, Gastropoda). J Exp Mar Biol Ecol 187:1–12CrossRefGoogle Scholar
  58. Meiklejohn CD, Montooth KL, Rand DM (2007) Positive and negative selection on the mitochondrial genome. Trends Genet 23:259–263CrossRefGoogle Scholar
  59. Metz EC, Robles-Sikisaka R, Vacquier VD (1998) Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. Proc Natl Acad Sci USA 95:10676–10681CrossRefGoogle Scholar
  60. Monmonier M (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261CrossRefGoogle Scholar
  61. Moore LB (1961) Distribution patterns of New Zealand seaweeds. Tuatara 9:18–23Google Scholar
  62. Naylor JR, McShane PE (1997) Predation by polychaete worms on larval and post-settlement abalone Haliotis iris (Mollusca: Gastropoda). J Exp Mar Biol Ecol 214:283–290CrossRefGoogle Scholar
  63. Naylor JR, McShane PE (2001) Mortality of post-settlement abalone Haliotis iris caused by conspecific adults and wave exposure. N Z J Mar Freshwater Res 35:363–369CrossRefGoogle Scholar
  64. Naylor JR, Manighetti BM, Neil HL, Kim SW (2007) Validated estimation of growth and age in the New Zealand abalone Haliotis iris using stable oxygen isotopes. Mar Freshw Res 58:354–362CrossRefGoogle Scholar
  65. Palumbi SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  66. Pawson DL (1961) Distribution patterns of New Zealand echinoderms. Tuatara 9:9–18Google Scholar
  67. Phillips NE, Shima JS (2006) Differential effects of suspended sediments on larval survival and settlement of New Zealand urchins Evechinus chloroticus and abalone Haliotis iris. Mar Ecol Prog Ser 314:149–158CrossRefGoogle Scholar
  68. Poore GCB (1973) Ecology of New Zealand abalones, Haliotis species (Mollusca: Gastropoda) 4. Reproduction. N Z J Mar Freshwater Res 7:67–84CrossRefGoogle Scholar
  69. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  70. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808CrossRefGoogle Scholar
  71. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45CrossRefGoogle Scholar
  72. Poulin E, Palma AT, Leiva G, Narvaez D, Pacheco R, Navarrete SA, Castilla JC (2002) Avoiding offshore transport of competent larvae during upwelling events: the case of the gastropod Concholepas concholepas in Central Chile. Limnol Oceanogr 47:1248–1255CrossRefGoogle Scholar
  73. Powell AWB (1961) New Zealand biotic provinces. Tuatara 9:1–8Google Scholar
  74. Rambaut A (2002) Se-Al v2.0a11 Carbon. University of Oxford, Oxford, UKGoogle Scholar
  75. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86CrossRefGoogle Scholar
  76. Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006CrossRefGoogle Scholar
  77. Roberts RD, Lapworth C (2001) Effect of delayed metamorphosis on larval competence, and post-larval survival and growth, in the abalone Haliotis iris Gmelin. J Exp Mar Biol Ecol 258:1–13CrossRefGoogle Scholar
  78. Roberts RD, Kaspar HF, Barker RJ (2004) Settlement of abalone (Haliotis iris) larvae in response to five species of coralline algae. J Shellfish Res 23:975–987Google Scholar
  79. Ross PM, Hogg ID, Pilditch CA, Lundquist CJ (2009) Phylogeography of New Zealand’s coastal benthos. N Z J Mar Freshwater Res 43:1009–1027CrossRefGoogle Scholar
  80. Roughgarden J, Gaines S, Possingham H (1988) Recruitment dynamics in complex life-cycles. Science 241:1460–1466CrossRefGoogle Scholar
  81. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386Google Scholar
  82. Sainsbury KJ (1982) Population dynamics and fishery management of the Paua, Haliotis iris.1. Population structure, growth, reproduction, and mortality. N Z J Mar Freshwater Res 16:147–161CrossRefGoogle Scholar
  83. Schiel DR (2004) The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons. J Exp Mar Biol Ecol 300:309–342CrossRefGoogle Scholar
  84. Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedPubMedCentralGoogle Scholar
  85. Shanks AL, Brink L (2005) Upwelling, downwelling, and cross-shelf transport of bivalve larvae: test of a hypothesis. Mar Ecol Prog Ser 302:1–12CrossRefGoogle Scholar
  86. Shirtcliffe TGL, Moore MI, Cole AG, Viner AB, Baldwin R, Chapman B (1990) Dynamics of the Cape Farewell upwelling plume, New Zealand. N Z J Mar Freshwater Res 24:555–568CrossRefGoogle Scholar
  87. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial-DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  88. Smith PJ, McVeagh MS (2006) Genetic population structure of black-foot paua. Research report for contract SAP2005–01, Ministry of Fisheries. Wellington, New ZealandGoogle Scholar
  89. Smith PJ, Macarthur GJ, Michael KP (1989) Regional variation in electromorph frequencies in the tuatua, Paphies subtriangulata, around New Zealand. N Z J Mar Freshwater Res 23:27–33CrossRefGoogle Scholar
  90. Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda JS, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375Google Scholar
  91. Star B, Apte S, Gardner JPA (2003) Genetic structuring among populations of the greenshell mussel Perna canaliculus revealed by analysis of randomly amplified polymorphic DNA. Mar Ecol Prog Ser 249:171–182CrossRefGoogle Scholar
  92. Stevens MI, Hogg ID (2004) Population genetic structure of New Zealand’s endemic corophiid amphipods: evidence for allopatric speciation. Biol J Linn Soc Lond 81:119–133CrossRefGoogle Scholar
  93. Stevens GR, McGlone M, McCulloch B (1995) Prehistoric New Zealand. Reed Publishing (NZ) Ltd., Auckland, New ZealandGoogle Scholar
  94. Swofford DL (1998) PAUP*, version 4b10: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  95. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  96. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  97. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence Data. 3. Cladogram estimation. Genetics 132:619–633PubMedPubMedCentralGoogle Scholar
  98. Tong LJ, Moss GA, Redfearn P, Illingworth J (1992) A manual of techniques for culturing paua, Haliotis iris, through to the early juvenile stage. MAF Technical Report No. 31. Ministry of Fisheries, Wellington, New ZealandGoogle Scholar
  99. Veale AJ (2007) Phylogeography of two intertidal benthic marine invertebrates around New Zealand, the waratah anemone (Actinia tenebrosa) and the snakeskin chiton (Sypharochiton pelliserpentis). Master Thesis, University of Auckland, Auckland, New ZealandGoogle Scholar
  100. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450CrossRefGoogle Scholar
  101. Waters JM, Roy MS (2004) Phylogeography of a high-dispersal New Zealand sea star: does upwelling block gene-flow? Mol Ecol 13:2797–2806CrossRefGoogle Scholar
  102. Withler RE, Campbell A, Li SR, Brouwer D, Supernault KJ, Miller KM (2003) Implications of high levels of genetic diversity and weak population structure for the rebuilding of northern abalone in British Columbia, Canada. J Shellfish Res 22:839–847Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Margaret Will
    • 1
  • Marie L. Hale
    • 1
  • David R. Schiel
    • 1
  • Neil J. Gemmell
    • 1
    • 2
    Email author
  1. 1.School of Biological SciencesUniversity of CanterburyChristchurchNew Zealand
  2. 2.Centre for Reproduction and Genomics, Department of Anatomy and Structural BiologyUniversity of OtagoDunedinNew Zealand

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