Biological Invasions

, Volume 15, Issue 1, pp 185–197 | Cite as

Low genetic and morphological differentiation between an introduced population of dunnocks in New Zealand and an ancestral population in England

  • Eduardo S. A. SantosEmail author
  • Ian G. Jamieson
  • Luana L. S. Santos
  • Shinichi Nakagawa
Original Paper


Species invasions and exotic species introductions can be considered as ‘unplanned experiments’, which help us to understand the evolution of organisms. In this study, we investigated whether an exotic bird species, the dunnock (Prunella modularis), has diverged genetically and morphologically from its native source population (Cambridge, England) after introduction into a new environment (Dunedin, South Island of New Zealand; exotic population). We used a set of microsatellite markers and three morphological traits to quantify the divergence between these two populations. We quantified neutral genotypic differentiation between the populations, and also used an individual-based Bayesian clustering method to assess genetic structure. We compared morphological divergence using univariate and principal components analyses. We found that individuals from the Dunedin population are genetically distinct from the Cambridge population, but levels of differentiation are very low. Overall within-population levels of genetic diversity are low compared to other bird species, and effective population sizes are small; indicating that the native population probably has a historically low level of genetic diversity, and that the introduced population retained most of that diversity after its introduction into New Zealand. We found little evidence of morphological divergence, and the evolutionary rate of change in these traits is below the average for other taxa. Our study adds support to the growing literature showing that invasive species maintain most of their initial genetic diversity after multiple founder events, even when population size is severely reduced. Moreover, our morphological data indicate slow evolutionary rates in species introduced to similar habitats.


Contemporary evolution Prunella modularis Exotic species Avian invasion Morphological divergence Evolutionary rate 



We would like to thank the University of Otago for a postgraduate scholarship to ESAS and for a Marsden grant (UOO-0812) to SN, and the Association for the Study of Animal Behaviour for a research grant. We thank the Dunedin Botanic Garden and its staff for allowing us to conduct our research on their grounds. We especially thank Losia Lagisz and Karin Ludwig for their extensive help with the genetic analyses, and Delphine Scheck, Patrick Crowe and Sam van der Horst for field assistance. We thank Nick Davies and Terry Burke for kindly providing data and samples from Cambridge dunnocks. We thank Radovan Jambor for providing information about Slovakian dunnocks. We thank Deborah Dawson, Andy Krupa, Daichi Saito and Isao Nishiumi for providing primer aliquots. Comments by Marcos R. Lima, Terry Burke and two anonymous reviewers greatly improved an early version of this manuscript.

Supplementary material

10530_2012_278_MOESM1_ESM.doc (106 kb)
Supplementary material 1 (DOC 106 kb)


  1. Badyaev AV, Hill GE (2000) The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution 54:1784–1794PubMedGoogle Scholar
  2. Baker A (1992) Genetic and morphometric divergence in ancestral European and descendent New Zealand populations of chaffinches (Fringilla coelebs). Evolution 46:1784–1800CrossRefGoogle Scholar
  3. Baker AJ, Moeed A (1987) Rapid genetic differentiation and founder effect in colonizing populations of common mynas (Acridotheres tristis). Evolution 41:525–538CrossRefGoogle Scholar
  4. Blackburn TM, Lockwood JL, Cassey P (2009) Avian invasions: the ecology and evolution of exotic birds. 320Google Scholar
  5. Briskie JV (2006) Introduced birds as model systems for the conservation of endangered native birds. Auk 123:949–957Google Scholar
  6. Briskie JV, Mackintosh M (2004) Hatching failure increases with severity of population bottlenecks in birds. Proc Nat Acad Sci 101:558–561PubMedCrossRefGoogle Scholar
  7. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455PubMedGoogle Scholar
  8. Budaev SV (2010) Using principal components and factor analysis in animal behaviour research: caveats and guidelines. Ethology 116:472–480CrossRefGoogle Scholar
  9. Burke T, Davies N, Bruford M, Hatchwell BJ (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251CrossRefGoogle Scholar
  10. Cabe PR (1998) The effects of founding bottlenecks on genetic variation in the European starling (Sturnus vulgaris) in North America. Heredity 80:519–525CrossRefGoogle Scholar
  11. Clegg S, Degnan S, Kikkawa J et al (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Nat Acad Sci 99:8127–8132PubMedCrossRefGoogle Scholar
  12. Congdon NM, Briskie JV (2010) Effect of population bottlenecks on the egg morphology of introduced birds in New Zealand. Ibis 152:136–144CrossRefGoogle Scholar
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  14. Cramp S (1988) The birds of the Western Palearctic. Oxford University Press, OxfordGoogle Scholar
  15. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557PubMedCrossRefGoogle Scholar
  16. Davies NB (1992) Dunnock behaviour and social evolutionGoogle Scholar
  17. Dawson DA, Horsburgh GJ, Küpper C et al (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility—as demonstrated for birds. Mol Ecol Resour 10:475–494PubMedCrossRefGoogle Scholar
  18. Duncan R, Blackburn T, Sol D (2003) The ecology of bird introductions. Annu Rev Ecol Evol Syst 34:71–98CrossRefGoogle Scholar
  19. Evans SR, Sheldon BC (2008) Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conserv Biol 22:1016–1025PubMedCrossRefGoogle Scholar
  20. Evans KL, Duncan R, Blackburn T, Crick H (2005) Investigating geographic variation in clutch size using a natural experiment. Funct Ecol 19:616–624CrossRefGoogle Scholar
  21. Evans KL, Gaston KJ, Frantz AC et al (2009) Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc Biol Sci 276:2403–2410PubMedCrossRefGoogle Scholar
  22. Evans KL, Hatchwell BJ, Parnell M, Gaston KJ (2010) A conceptual framework for the colonisation of urban areas: the blackbird Turdus merula as a case study. Biol Rev 85:643–667PubMedGoogle Scholar
  23. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to Conservation Genetics, 2nd edn, p 642Google Scholar
  24. Goodenough AE, Stafford R, Catlin-Groves CL, Smith AL, Hart AG (2010) Within-and among-observer variation in measurements of animal biometrics and their influence on accurate quantification of common biometric-based condition indices. Ann Zool Fenn 47:323–334CrossRefGoogle Scholar
  25. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  26. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22Google Scholar
  27. Haldane JBS (1949) Suggestions as to quantitative measurement of rates of evolution. Evolution 3:51–56PubMedCrossRefGoogle Scholar
  28. Harrison CJO (1982) An atlas of the birds of the Western Palaearctic, 1st ednGoogle Scholar
  29. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29PubMedCrossRefGoogle Scholar
  30. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  31. Holt RD, Barfield M, Gomulkiewicz R (2005) Theories of niche conservatism and evolution: could exotic species be potential tests? In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland, pp 259–290Google Scholar
  32. Jamieson IG (2011) Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conserv Biol 25:115–123PubMedCrossRefGoogle Scholar
  33. Johnston RF, Selander RK (1964) House sparrows: rapid evolution of races in North America. Science 144:550–552CrossRefGoogle Scholar
  34. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  35. Kekkonen J, Seppä P, Hanski IK et al (2011) Low genetic differentiation in a sedentary bird: house sparrow population genetics in a contiguous landscape. Heredity 106:183–190PubMedCrossRefGoogle Scholar
  36. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112–113:145–164PubMedCrossRefGoogle Scholar
  37. Lomolino MV (1985) Body size of mammals on islands: the island rule reexamined. Am Nat 125:310–316CrossRefGoogle Scholar
  38. Long JL (1981) Introduced birds of the worldGoogle Scholar
  39. Mathys BA, Lockwood JL (2009) Rapid evolution of great kiskadees on Bermuda: an assessment of the ability of the Island rule to predict the direction of contemporary evolution in exotic vertebrates. J Biogeogr 36:2204–2211CrossRefGoogle Scholar
  40. Mathys BA, Lockwood JL (2011) Contemporary morphological diversification of passerine birds introduced to the Hawaiian archipelago. Proc R Soc Lond B Biol Sci 278:2392–2400CrossRefGoogle Scholar
  41. Merilä J, Björklund M, Baker AJ (1996) The successful founder: genetics of introduced Carduelis chloris (greenfinch) populations in New Zealand. Heredity 77:410–422CrossRefGoogle Scholar
  42. Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  43. Nicholls J, Double M, Rowell D, Magrath R (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176CrossRefGoogle Scholar
  44. Olson VA, Davies RG, Orme CDL et al (2009) Global biogeography and ecology of body size in birds. Ecol Lett 12:249–259PubMedCrossRefGoogle Scholar
  45. Otago Acclimatisation Society (1865) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  46. Otago Acclimatisation Society (1873) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  47. Otago Acclimatisation Society (1878) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  48. Otago Acclimatisation Society (1880) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  49. Otago Acclimatisation Society (1886) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  50. Otago Acclimatisation Society (1891) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  51. Otago Acclimatisation Society (1896) Annual report. Otago Acclimatisation Society, DunedinGoogle Scholar
  52. Paradis E, Baillie SR, Sutherland WJ, Gregory RD (1998) Patterns of natal and breeding dispersal in birds. J Anim Ecol 67:518–536CrossRefGoogle Scholar
  53. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  54. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  55. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  56. Rasner C, Yeh P, Eggert L et al (2004) Genetic and morphological evolution following a founder event in the dark-eyed junco, Junco hyemalis thurberi. Mol Ecol 13:671–681PubMedCrossRefGoogle Scholar
  57. Raymond M, Rousset F (1995) Genepop (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  58. Revelle W (2011) psych: procedures for psychological, psychometric, and personality research, pp 1–244Google Scholar
  59. Robinson RA (2005) BirdFacts: profiles of birds occurring in Britain & Ireland. BTO, ThetfordGoogle Scholar
  60. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedCrossRefGoogle Scholar
  61. Ross H (1983) Genetic differentiation of starling (Sturnus vulgaris: aves) populations in New Zealand and Great Britain. J Zool 201:351–362CrossRefGoogle Scholar
  62. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  63. Saito D, Nishiumi I, Nakamura M (2001) Characterization of nine polymorphic microsatellite loci from the alpine accentor Prunella collaris. Mol Ecol Notes 1:258–259CrossRefGoogle Scholar
  64. Santos ESA (2012) Discovery of previously unknown historical records on the introduction of dunnocks (Prunella modularis) into Otago, New Zealand during the 19th century. Notornis 59:79–81Google Scholar
  65. Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471PubMedCrossRefGoogle Scholar
  66. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst:393–430Google Scholar
  67. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101CrossRefGoogle Scholar
  68. 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
  69. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  70. Thomson GM (1922) The naturalisation of plants and animals in New Zealand. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  71. Uller T, Leimu R (2011) Founder events predict changes in genetic diversity during human-mediated range expansions. Global Change Biol 17:3478–3485CrossRefGoogle Scholar
  72. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  73. Van Valen L (1973) Pattern and the balance of nature. Evol Theory 1:31–49Google Scholar
  74. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756PubMedCrossRefGoogle Scholar
  75. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Eduardo S. A. Santos
    • 1
    Email author
  • Ian G. Jamieson
    • 1
  • Luana L. S. Santos
    • 1
  • Shinichi Nakagawa
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Department of Behavioural Ecology and Evolutionary GeneticsMax Planck Institute for OrnithologySeewiesenGermany

Personalised recommendations