Evolutionary Ecology

, Volume 27, Issue 2, pp 381–391 | Cite as

Limited genetic differentiation between acoustically divergent populations of urban and rural silvereyes (Zosterops lateralis)

  • Dominique A. PotvinEmail author
  • Kirsten M. Parris
  • Raoul A. Mulder
Original Paper


The bioacoustic attributes of vocalisations made by birds in urban environments often differ markedly from those of rural conspecifics. Whether such differences are result from genetic divergence between urban and rural populations, or from plasticity or cultural evolution of song remains poorly understood. Silvereyes (Zosterops lateralis) show evidence of acoustic adaptation to urban noise, modifying both their songs and calls in cities when compared to rural areas. We investigated whether these differences were associated with corresponding morphological and neutral genetic differences. Across six pairs of geographically separate urban and rural populations, all morphological traits measured were similar. Furthermore, genetic analyses of variation at nine microsatellite loci revealed high levels of genetic connectivity between populations, and similar levels of heterozygosity in both habitat types. Consistent directional shifts in song attributes of city birds across large geographic areas thus do not appear to be accompanied by associated morphological or neutral genetic divergence.


Urbanization Silvereye Population genetics Zosterops lateralis 



We thank three anonymous reviewers for helpful comments improving the manuscript. We thank J. Kruckel for field assistance, G. Fry, A. Leishman, D. Paton, D. Williams, E. Woehler, R. Fuller, and A. Fletcher for assistance in locating and banding, the Australian National Botanic Gardens (ACT), Namadgi National Park (ACT), Glenorchy City Council (Tas), Brisbane City Council (Qld), Munghorn Gap Nature Reserve (NSW), Kogarah City Council (NSW), Darebin City Council (Vic) and Darebin Parklands Association (Vic) for permission to conduct work on their lands.

Ethical note

Procedures were undertaken with the approval of the following agencies: Animal Ethics Committee at the University of Melbourne, Director-General’s Animal Care and Ethics Committee at the NSW Department of Primary Industries, and Wildlife Ethics Committee at the SA Department for Environment and Heritage.

Supplementary material

10682_2012_9591_MOESM1_ESM.doc (56 kb)
Supplementary material 1 (DOC 56 kb)
10682_2012_9591_MOESM2_ESM.pdf (999 kb)
Figure S1. Mean measurements of head-bill length, wing length, tarsus length, tail length and mass of rural and urban silvereyes, grouped by geographic area (indicated on map). Error bars represent standard deviation. (PDF 999 kb)


  1. Badyaev AV, Young RL, Oh KP, Addison C (2008) Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats. Evolution 62:1951–1964PubMedCrossRefGoogle Scholar
  2. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165PubMedCrossRefGoogle Scholar
  3. Blondel J (2007) Coping with habitat heterogeneity: the story of Mediterranean blue tits. J Ornithol 148:3–15CrossRefGoogle Scholar
  4. Cardoso GC, Atwell JW (2011) Directional cultural change by modification and replacement of memes. Evolution 65:295–300PubMedCrossRefGoogle Scholar
  5. Catterall CP, Wyatt WS, Henderson LJ (1982) Food resources, territory density and reproductive success of an island silvereye population Zosterops lateralis. Ibis 124:405–421CrossRefGoogle Scholar
  6. Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69CrossRefGoogle Scholar
  7. Chan K, Kikkawa J (1997) Short communication: a silvereye Dilemma: to migrate or not to migrate? Emu 97:91–93CrossRefGoogle Scholar
  8. Clegg SM, Degnan SM, Moritz C, Estoup A, Kikkawa J, Owens IP (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–2099PubMedGoogle Scholar
  9. Cynx J, Bean NJ, Rossman I (2005) Testosterone implants alter the frequency range of zebra finch songs. Horm Behav 47:446–451PubMedCrossRefGoogle Scholar
  10. Degnan SM, Robertson BC, Clegg SM, Moritz CC (1999) Microsatellite primers for studies of gene flow and mating systems in white-eyes (Zosterops). Mol Ecol 8:159–160PubMedCrossRefGoogle Scholar
  11. Derryberry EP (2009) Ecology shapes birdsong evolution: variation in morphology and habitat explains variation in white-crowned sparrow song. Am Nat 174:24–33PubMedCrossRefGoogle Scholar
  12. DiBattista J (2008) Patterns of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156CrossRefGoogle Scholar
  13. Edelaar P, Benkman CW (2006) Replicated population divergence caused by localized coevolution? A test of three hypotheses in the red crossbill-lodgepole pine system. J Evolut Biol 19:1651–1659CrossRefGoogle Scholar
  14. Evans KL, Gaston KJ, Frantz AC, Simeoni M, Sharp SP, McGowan A, Dawson DA, Walasz K, Partecke J, Burke T, Hatchwell BJ (2009) Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc R Soc B Biol Sci 276:2403–2410CrossRefGoogle Scholar
  15. Evans KL, Newton J, Gaston KJ, Sharp SP, McGowan A, Hatchwell BJ (2012) Colonisation of urban environments is associated with reduced migratory behaviour, facilitating divergence from ancestral populations. Oikos 121:634–640CrossRefGoogle Scholar
  16. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolut Bioinform Online 1:47–50Google Scholar
  17. Frentiu FD, Lange CL, Burke T, Owens IPF (2003) Isolation of microsatellite loci in the Capricorn silvereye, Zosterops lateralis chlorocephalus (Aves: Zosteropidae). Mol Ecol Notes 3:462–464CrossRefGoogle Scholar
  18. Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  19. Halfwerk W, Slabbekoorn H (2009) A behavioural mechanism explaining noise-dependent frequency use in urban birdsong. Anim Behav 78:1301–1307CrossRefGoogle Scholar
  20. Higgins PJ, Peter JM, Cowling SJ (2006) Boatbill to starlings: handbook of Australian, New Zealand and antarctic birds, vol 7. Oxford University Press, MelbourneGoogle Scholar
  21. Jost LOU (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091CrossRefGoogle Scholar
  22. Kikkawa J (1987) Social relations and fitness in silvereyes. In: Ito Y, Brown J, Kikkawa J (eds) Animal societies—theories and facts. Japan Scientific Press, Tokyo, pp 253–266Google Scholar
  23. Kikkawa J, Wilson J (1983) Breeding and dominance among the Heron Island Silvereyes Zosterops lateralis chlorocephala. Emu 83:181–198CrossRefGoogle Scholar
  24. Laitinen J, Samarut J, Hölttä E (1994) A nontoxic and versatile protein salting-out method for isolation of DNA. Biotechniques 17:316–322PubMedGoogle Scholar
  25. Leader N, Geffen E, Mokady O, Yom-Tov Y (2008) Song dialects do not restrict gene flow in an urban population of the orange-tufted sunbird, Nectarinia osea. Behav Ecol Sociobiol 62:1299–1305CrossRefGoogle Scholar
  26. Luther D, Baptista L (2010) Urban noise and the cultural evolution of bird songs. Proc R Soc Lond B 277:469–473CrossRefGoogle Scholar
  27. MacDougall-Shackleton EA, MacDougall-Shackleton SA (2001) Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure. Evolution 55:2568–2575PubMedGoogle Scholar
  28. Marler P (2004) Bird calls: their potential for behavioral neurobiology. Ann N Y Acad Sci 1016:31–44PubMedCrossRefGoogle Scholar
  29. McCarthy MA (2007) Bayesian methods for ecology. University Press, CambridgeCrossRefGoogle Scholar
  30. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402PubMedGoogle Scholar
  31. Meirmans PG, Van Tienderen PH (2004) Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  32. Nemeth E, Brumm H (2010) Birds and anthropogenic noise: are urban songs adaptive? Am Nat 176:465–475PubMedCrossRefGoogle Scholar
  33. Partecke J, Gwinner E (2007) Increased sedentariness in European blackbirds following urbanization: a consequence of local adaptation? Ecology 88:882–890PubMedCrossRefGoogle Scholar
  34. Partecke J, Van’t Hof T, Gwinner E (2004) Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? Proc R Soc B 271:1995–2001PubMedCrossRefGoogle Scholar
  35. Partecke J, Gwinner E, Bensch S (2006) Is urbanisation of European blackbirds (Turdus merula) associated with genetic differentiation? J Ornithol 147:549–552CrossRefGoogle Scholar
  36. Patricelli GL, Blickley JL (2006) Avian communication in urban noise: causes and consequences of vocal adjustment. Auk 123:639–649CrossRefGoogle Scholar
  37. Patten MA, Rotenberry JT, Zuk M (2004) Habitat selection, acoustic adaptation, and the evolution of reproductive isolation. Evolution 58:2144–2155PubMedGoogle Scholar
  38. Podos J, Southall JA, Rossi-Santos MR (2004) Vocal mechanics in Darwin’s finches: correlation of beak gape and song frequency. J Exp Biol 207:607–619PubMedCrossRefGoogle Scholar
  39. Potvin DA, Parris KM, Mulder RA (2011) Geographically pervasive effects of urban noise on frequency and syllable rate of songs and calls in silvereyes (Zosterops lateralis). Proc R Soc B Biol Sci 278:2464–2469CrossRefGoogle Scholar
  40. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  41. Rice WR (1987) Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character. Evolut Ecol 1:301–314CrossRefGoogle Scholar
  42. Riede T, Suthers RA, Fletcher NH, Blevins WE (2006) Songbirds tune their vocal tract to the fundamental frequency of their song. Proc Natl Acad Sci 103:5543–5548PubMedCrossRefGoogle Scholar
  43. Ripmeester EA, Kok JS, van Rijssel JC, Slabbekoorn H (2010) Habitat-related birdsong divergence: a multi-level study on the influence of territory density and ambient noise in European blackbirds. Behav Ecol Sociobiol 64:409–418PubMedCrossRefGoogle Scholar
  44. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  45. Slabbekoorn H, Ripmeester EA (2008) Birdsong and anthropogenic noise: implications and applications for conservation. Mol Ecol 17:72–83PubMedCrossRefGoogle Scholar
  46. Slabbekoorn H, Smith TB (2002a) Bird song, ecology and speciation. Philos Trans R Soc Lond B Biol Sci 357:493–503PubMedCrossRefGoogle Scholar
  47. Slabbekoorn H, Smith TB (2002b) Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution 56:1849–1858PubMedGoogle Scholar
  48. Spiegelhalter D, Thomas A, Best N, Lunn D (2006) OPENBUGS user manual version 220. MRC Biostatistics Unit, CambridgeGoogle Scholar
  49. Vangestel C, Mergeay J et al (2011) Spatial heterogeneity in genetic relatedness among house sparrows along an urban–rural gradient as revealed by individual-based analysis. Mol Ecol 20(22):4643–4653Google Scholar
  50. Yoktan K, Geffen E, Ilany A, Yom-Tov Y, Naor A, Leader N (2011) Vocal dialect and genetic subdivisions along a geographic gradient in the orange-tufted sunbird. Behav Ecol Sociobiol 65:1389–1402CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Dominique A. Potvin
    • 1
    Email author
  • Kirsten M. Parris
    • 2
  • Raoul A. Mulder
    • 1
  1. 1.Department of ZoologyUniversity of MelbourneParkvilleAustralia
  2. 2.School of BotanyUniversity of MelbourneParkvilleAustralia

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