Conservation Genetics

, Volume 8, Issue 3, pp 705–714

Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges

  • Sanne Boessenkool
  • Sabrina S. Taylor
  • Carolyn K. Tepolt
  • Jan Komdeur
  • Ian G. Jamieson
Original Paper

Abstract

For conservation purposes islands are considered safe refuges for many species, particularly in regions where introduced predators form a major threat to the native fauna, but island populations are also known to possess low levels of genetic diversity. The New Zealand archipelago provides an ideal system to compare genetic diversity of large mainland populations where introduced predators are common, to that of smaller offshore islands, which serve as predator-free refuges. We assessed microsatellite variation in South Island robins (Petroica australis australis), and compared large mainland, small mainland, natural island and translocated island populations. Large mainland populations exhibited more polymorphic loci and higher number of alleles than small mainland and natural island populations. Genetic variation did not differ between natural and translocated island populations, even though one of the translocated populations was established with five individuals. Hatching failure was recorded in a subset of the populations and found to be significantly higher in translocated populations than in a large mainland population. Significant population differentiation was largely based on heterogeneity in allele frequencies (including fixation of alleles), as few unique alleles were observed. This study shows that large mainland populations retain higher levels of genetic diversity than natural and translocated island populations. It highlights the importance of protecting these mainland populations and using them as a source for new translocations. In the future, these populations may become extremely valuable for species conservation if existing island populations become adversely affected by low levels of genetic variation and do not persist.

Keywords

Genetic variation New Zealand Bottleneck Population differentiation Petroica australis australis 

References

  1. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265PubMedCrossRefGoogle Scholar
  2. Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Philos Trans R Soc Lond B Biol Sci 353:177–186PubMedCrossRefGoogle Scholar
  3. Ardern SL, Lambert DM, Rodrigo AG, Mclean IG (1997) The effects of population bottlenecks on multilocus DNA variation in robins. J Hered 88:179–186Google Scholar
  4. Armstrong DP, Ewen JG, Dimond WJ, Lovegrove T, Bergström A, Walter B (2000) Breeding biology of North Island robins (Petroica australis longipes) on Tiritiri Matangi Island, Hauraki Gulf, New Zealand. Notornis 47:106–118Google Scholar
  5. Armstrong DP, Mclean IG (1995) New Zealand translocation: theory and practice. Pac Conserv Biol 2:39–54Google Scholar
  6. Belkhir K, Porsa P, Chikhi L, Raufaste N, Bonhomme F (2004) Genetix v. 4.05, Logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, MontpellierGoogle Scholar
  7. Bell BD (1991) Recent avifaunal changes and the history of ornithology in New Zealand. Acta XX Congressus Internationalis Ornithologici. 195–230Google Scholar
  8. Bensch S, Price T, Kohn J (1997) Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol Ecol 6:91–92PubMedCrossRefGoogle Scholar
  9. Bull PC, Gaze PD, Robertson CJR (1985) The atlas of bird distribution in New Zealand. Ornithological Society of New Zealand, WellingtonGoogle Scholar
  10. Butler D (2003) Rotoiti Nature Recovery Project 2000–2001 Annual Report. Department of Conservation, NelsonGoogle Scholar
  11. Byrne AJ (1999) Effects of population bottlenecks on the South Island robin, Petroica australis australis. Ph.D. thesis, University of Canterbury, Christchurch, New ZealandGoogle Scholar
  12. Chakraborty R, Nei M (1977) Bottleneck effects on average heterozygosity and genetic distance with the stepwise mutation model. Evolution 31:347–356CrossRefGoogle Scholar
  13. Clout M (2001) Where protection is not enough: active conservation in New Zealand. Trends Ecol Evol 16:415–416CrossRefGoogle Scholar
  14. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270PubMedCrossRefGoogle Scholar
  15. Dilks P, Willans M, Pryde M, Fraser I (2003) Large scale stoat control to protect mohua (Mohoua ochrocephala) and kaka (Nestor meridionalis) in the Eglinton Valley, Fiordland, New Zealand. NZ J Ecol 27:1–9Google Scholar
  16. Dowling DK, Adcock J, Mulder RA (2003) Novel polymorphic microsatellite markers for paternity analysis in the red-capped robin (Petroica goodenovii: Aves). Mol Ecol Notes 3:517–519CrossRefGoogle Scholar
  17. Duncan PJ, Webb PI, Palmeirim JM (1999) Distribution of New Zealand robin in a forest mosaic. Emu 99:222–226CrossRefGoogle Scholar
  18. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  19. Eldridge MDB, Kinnear JE, Zenger KR, McKenzie LM, Spencer PBS (2004) Genetic diversity in remnant mainland and “pristine” island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus and Petrogale lateralis. Conserv Genet 5:325–338CrossRefGoogle Scholar
  20. Etheridge N, Powlesland RG (2001) High productivity and nestling success of South Island robins (Petroica australia australis) following predator control at St Arnaud, Nelson Lakes, South Island. Notornis 48:179–180Google Scholar
  21. Flack JAD (1974) Chatham Island black robin. Wildl—a Rev, NZ Wildl Serv 5:25–34Google Scholar
  22. Flack JAD (1979) Biology and ecology of the South Island robin. In: Hunt DM, Gill BJ (eds) Ecology of Kowhai Bush. Kaikoura, University of Canterbury, pp 22–26Google Scholar
  23. Fleming CA (1950) New Zealand flycatchers of the genus Petroica Swainson (Aves), Part 1 and 2. Trans Roy Soc NZ 78:14–47, 126–160Google Scholar
  24. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327PubMedCrossRefGoogle Scholar
  25. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327PubMedCrossRefGoogle Scholar
  26. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  27. Gibbs M, Dawson DA, McCamley C, Wardle AF, Armour JAL, Burke T (1997) Chicken microsatellite markers isolated from libraries enriched for simple tandem repeats. Anim Genet 28:401–417PubMedCrossRefGoogle Scholar
  28. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Institute of Ecology, LausanneGoogle Scholar
  29. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  30. Hanotte O, Zanon C, Pugh A, Greig C, Dixon A, Burke T (1994) Isolation and characterization of microsatellite loci in a passerine bird—the reed bunting Emberiza schoeniclus. Mol Ecol 3:529–530PubMedGoogle Scholar
  31. Heather B, Robertson H (1996) Field guide to the birds of New Zealand. Viking AucklandGoogle Scholar
  32. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Ann Rev Ecol Syst 31:139–162CrossRefGoogle Scholar
  33. Hill GS (2005) Operation ark—operational plan for predator control and monitoring in the Eglinton Valley, Fiordland National Park. Department of Conservation, Te Anau, Unpublished reportGoogle Scholar
  34. Jamieson IG, Roy MS, Lettink M (2003) Sex-specific consequences of recent inbreeding in an ancestrally inbred population of New Zealand takahe. Conserv Biol 17:708–716CrossRefGoogle Scholar
  35. Jamieson IG, Wallis GP, Briskie JV (2006) Inbreeding and endangered species management: is New Zealand out-of-step with the rest of the world? Conserv Biol 20:38–47PubMedCrossRefGoogle Scholar
  36. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  37. Lambert DM, King T, Shepherd LD, Livingston A, Anderson S, Craig JL (2005) Serial population bottlenecks and genetic variation: translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufusater). Conserv Genet 6:1–14CrossRefGoogle Scholar
  38. Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437CrossRefGoogle Scholar
  39. Mackintosh MA, Briskie JV (2005) High levels of hatching failure in an insular population of the South Island robin: a consequence of food limitation? Biol Conserv 122:409–416CrossRefGoogle Scholar
  40. Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  41. Merilä J, Björklund M, Baker AJ (1996) The successful founder: genetics of introduced Carduelis chloris (greenfinch) populations in New Zealand. Heredity 77:410–422Google Scholar
  42. Miller HC (2003) Evolutionary genetics and the major histocompatibility complex of New Zealand Robins (Petroicidae). Ph.D. thesis, Massey UniversityGoogle Scholar
  43. Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721PubMedCrossRefGoogle Scholar
  44. Mills HR, Moro D, Spencer PBS (2004) Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia. Anim Conserv 7:387–395CrossRefGoogle Scholar
  45. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  46. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  47. Oppel S (2000) Reintroduction of threatened bird species to the predator free lowland forest of Ulva Island. Department of Conservation, InvercargillGoogle Scholar
  48. Oppel S, Beaven B (2002) Stewart Island robins (Petroica australis rakiura) fly home after transfer to Ulva Island. Notornis 49:180–181Google Scholar
  49. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  50. Powlesland RG (1983) Breeding and mortality of the South Island robin in Kowhai Bush, Kaikoura. Notornis 30:265–282Google Scholar
  51. Raymond M, Rousset F (1995) Genepop (version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  52. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  53. Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T (2000) Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 9:2226–2231PubMedCrossRefGoogle Scholar
  54. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 13:1219–1228Google Scholar
  55. Sefc KM, Payne RB, Sorenson MD (2001) Characterization of microsatellite loci in village indigobirds Vidua chalybeata and cross-species amplification in estrildid and ploceid finches. Mol Ecol Notes 1:252–254CrossRefGoogle Scholar
  56. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  57. Sjögren P, Wyöni PI (1994) Conservation genetics and detection of rare alleles in finite populations. Conserv Biol 8:267–270CrossRefGoogle Scholar
  58. Suzuki DT, Griffiths AJF, Lewontin RC (1981) An introduction to genetic analysis, 2 edn. W.H. Freeman and Company, San FransiscoGoogle Scholar
  59. Tarr CL, Conant S, Fleischer RC (1998) Founder events and variation at microsatellite loci in an insular passerine bird, the Laysan finch (Telespiza cantans). Mol Ecol 7:719–731CrossRefGoogle Scholar
  60. Taylor SS, Jamieson IG, Armstrong DP (2005) Successful island reintroductions of New Zealand robins and saddlebacks with small numbers of founders. Anim Conserv 8:415–420CrossRefGoogle Scholar
  61. Templeton AR, Read B (1994) Inbreeding: one word, several meanings, much confusion. In: Loeschcke V, Tomiuk J, Jain SK (eds) Conserv Genet Birkhäuser Verlag, Basel pp 91–105Google Scholar
  62. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  63. Wright S (1969) The theory of gene frequencies. University of Chicago Press, ChicagoGoogle Scholar
  64. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall International, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Sanne Boessenkool
    • 1
    • 2
  • Sabrina S. Taylor
    • 1
  • Carolyn K. Tepolt
    • 1
  • Jan Komdeur
    • 2
  • Ian G. Jamieson
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Animal Ecology GroupCentre for Evolutionary and Ecological Studies, University of GroningenHarenThe Netherlands

Personalised recommendations