Genetic divergence of early song discrimination between two young songbird species


Juvenile songbirds express species-specific song discrimination from an early age, which focuses learning onto the songs of their parental species. However, it remains unknown whether this early song discrimination is influenced by early social experience or maternal effects or whether it is instead largely genetically determined. We manipulated early social experience by swapping young embryos between the nests of two co-occurring songbird species—pied and collared flycatchers. We show that nestlings are more active in response to playbacks of conspecific songs, even when raised by adults from the other species, thus enabling us to reject social experience as the main determinant of early song discrimination. We then crossed the two species in captivity and showed that the song responses of hybrid nestlings do not depend on social experience or maternal species, implying genetic divergence of early song discrimination. Our results provide conclusive evidence that early song discrimination has a largely genetic component, which can stabilize reproductive isolation by reducing song learning across closely related species.

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Figure 1: Overview of the song learning process from embryo to adulthood.
Figure 2: Song playbacks to nestling collared and pied flycatchers.
Figure 3: Hybrid nestling experiment results.


  1. 1

    Bolhuis, J. J., Okanoya, K. & Scharr, C. Twitter evolution: converging mechanisms in birdsong and human speech. Nat. Rev. Neurosci. 11, 747–759 (2010).

    CAS  PubMed  Article  Google Scholar 

  2. 2

    Price, T. Speciation in Birds (Roberts and Company Publishers, 2008).

    Google Scholar 

  3. 3

    Lemaire, F. Mixed song, interspecific competition and hybridisation in the reed and marsh warblers (Acrocephalus scirpaceus and palustris). Behaviour 63, 215–240 (1977).

    Article  Google Scholar 

  4. 4

    Helb, H.-W., Dowsett-Lemaire, F., Bergmann, H.-H. & Conrads, K. Mixed singing in European songbirds—a review. Z. Tierpsychol. 69, 27–41 (1985).

    Article  Google Scholar 

  5. 5

    Haavie, J. et al. Flycatcher song in allopatry and sympatry—convergence, divergence and reinforcement. J. Evol. Biol. 17, 227–237 (2004).

    CAS  PubMed  Article  Google Scholar 

  6. 6

    Qvarnström, A., Haavie, J., Sæther, S. A., Eriksson, D. & Pärt, T. Song similarity predicts hybridization in flycatchers. J. Evol. Biol. 19, 1202–1209 (2006).

    PubMed  Article  Google Scholar 

  7. 7

    Nelson, D. A. & Marler, P. Innate recognition of song in white-crowned sparrows: a role in selective vocal learning? Anim. Behav. 46, 806–808 (1993).

    Article  Google Scholar 

  8. 8

    Whaling, C. S., Solis, M. M., Doupe, A. J., Soha, J. A. & Marler, P. Acoustic and neural bases for innate recognition of song. Proc. Natl Acad. Sci. USA 94, 12694–12698 (1997).

    CAS  PubMed  Article  Google Scholar 

  9. 9

    Braaten, R. F. & Reynolds, K. Auditory preference for conspecific song in isolation-reared zebra finches. Anim. Behav. 58, 105–111 (1999).

    CAS  PubMed  Article  Google Scholar 

  10. 10

    Amin, N., Doupe, A. & Theunissen, F. E. Development of selectivity for natural sounds in the songbird auditory forebrain. J. Neurophysiol. 97, 3517–3531 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  11. 11

    Adret, P., Meliza, C. D. & Margoliash, D. Song tutoring in presinging zebra finch juveniles biases a small population of higher-order song-selective neurons toward the tutor song. J. Neurophysiol. 108, 1977–1987 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  12. 12

    Hauber, M. E., Woolley, S. M., Cassey, P. & Theunissen, F. E. Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds. Behav. Brain Res. 243, 184–190 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13

    Shizuka, D. Early song discrimination by nestling sparrows in the wild. Anim. Behav. 92, 19–24 (2014).

    Article  Google Scholar 

  14. 14

    McFarlane, S. E., Söderberg, A., Wheatcroft, D. & Qvarnström, A. Song discrimination by nestling collared flycatchers during early development. Biol. Lett. 12, 20160234 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  15. 15

    Marler, P. & Peters, S. Selective vocal learning in a sparrow. Science 198, 519–521 (1977).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. 16

    Marler, P. Three models of song learning: evidence from behavior. J. Neurobiol. 33, 501–516 (1997).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. 17

    Clayton, N. S. The effects of cross-fostering on selective song learning in estrildid finches. Behaviour 109, 163–175 (1989).

    Article  Google Scholar 

  18. 18

    Wright, T. F., Brittan–Powell, E. F., Dooling, R. J. & Mundinger, P. C. Sex-linked inheritance of hearing and song in the Belgian waterslager canary. Proc. R. Soc. Lond. B 271, S409–S412 (2004).

    Google Scholar 

  19. 19

    Colombelli-Négrel, D. et al. Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr. Biol. 22, 2155–2160 (2012).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  20. 20

    Colombelli-Négrel, D., Hauber, M. E. & Kleindorfer, S. Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos. Proc. R. Soc. Lond. B 281, 20141154 (2014).

    Article  Google Scholar 

  21. 21

    Mariette, M. M. & Buchanan, K. L. Prenatal acoustic communication programs offspring for high temperatures in a songbird. Science 353, 812–814 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  22. 22

    Grant, B. R & Grant, P. R. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. H. ) 404–422 (Oxford Univ. Press, 1998).

    Google Scholar 

  23. 23

    Johannessen, L. E., Slagsvold, T. & Hansen, B. T. Effects of social rearing conditions on song structure and repertoire size: experimental evidence from the field. Anim. Behav. 72, 83–95 (2006).

    Article  Google Scholar 

  24. 24

    Groothius, T. G., Muller, W., von Engelhardt, N., Carere, C. & Eising, C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329–352 (2005).

    Article  CAS  Google Scholar 

  25. 25

    Metzger, D. C. H. & Schulte, P. M. Maternal stress has divergent effects on gene expression patterns in the brains of male and female threespine stickleback. Proc. R. Soc. Lond. B 283, (2016).

  26. 26

    Brenowitz, E. A. Testosterone and BDNF interactions in the avian song control system. Neuroscience 239, 115–123 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27

    Qvarnström, A., Rice, A. M. & Ellegren, H. Speciation in Ficedula flycatchers. Phil. Trans. R. Soc. Lond. B 365, 1841–1852 (2010).

    Article  Google Scholar 

  28. 28

    Eriksen, A., Slagsvold, T. & Lampe, H. M. Vocal plasticity—are pied flycatchers, Ficedula hypoleuca, open-ended learners? Ethology 117, 188–198 (2011).

    Article  Google Scholar 

  29. 29

    Chen, C. C., Winkler, C. M., Pfenning, A. R. & Jarvis, E. D. Molecular profiling of the developing avian telencephalon: regional timing and brain subdivision continuities. J. Comp. Neurol. 521, 3666–3701 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  30. 30

    Sheldon, B. C, Merilä, J., Qvarnström, A., Gustafsson, L. & Ellegren, H. Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc. R. Soc. Lond. B 264, 297–302 (1997).

    Article  Google Scholar 

  31. 31

    Maurer, G., Magrath, R. D., Leonard, M. L., Horn, A. G. & Donnelly, C. Begging to differ: scrubwren nestlings beg to alarm calls and vocalize when parents are absent. Anim. Behav. 65, 1045–1055 (2003).

    Article  Google Scholar 

  32. 32

    Sæther, S. A. et al. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318, 95–97 (2007).

    PubMed  Article  CAS  Google Scholar 

  33. 33

    Verzijden, M. N. et al. The impact of learning on sexual selection and speciation. Trends Ecol. Evol. 27, 511–519 (2012).

    PubMed  Article  Google Scholar 

  34. 34

    Nottebohm, F. et al. Song learning in birds: the relation between perception and production. Phil. Trans. R. Soc. Lond. B 329, 115–124 (1990).

    CAS  Article  Google Scholar 

  35. 35

    Riebel, K., Smallegange, I. M., Terpstra, N. J. & Bolhuis, J. J. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc. R. Soc. Lond. B 269, 729–733 (2002).

    Article  Google Scholar 

  36. 36

    Searcy, W. A. & Brenowitz, E. A. Sexual differences in species recognition of avian song. Nature 331, 152–154 (1988).

    Article  Google Scholar 

  37. 37

    Brittan-Powell, E. F., Dooling, R. F., Ryals, B. & Gleich, O. Electrophysiological and morphological development of the inner ear in Belgian waterslager canaries. Hear. Res. 269, 56–69 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  38. 38

    Nelson, D. A. A preference for own-subspecies’ song guides vocal learning in a song bird. Proc. Natl Acad. Sci. USA 97, 13348–13353 (2000).

    CAS  PubMed  Article  Google Scholar 

  39. 39

    Gorissen, L., Gorissen, M. & Eens, M. Heterospecific song matching in two closely related songbirds (Parus major and P. caeruleus): great tits match blue tits but not vice versa. Behav. Ecol. Sociobiol. 60, 260–269 (2006).

    Article  Google Scholar 

  40. 40

    Clayton, N. S. Subspecies recognition and song learning in zebra finches. Anim. Behav. 40, 1009–1017 (1990).

    Article  Google Scholar 

  41. 41

    Eriksen, A., Lampe, H. M. & Slagsvold, T. Interspecific cross-fostering affects song acquisition but not mate choice in pied flycatchers, Ficedula hypoleuca. Anim. Behav. 78, 857–863 (2009).

    Article  Google Scholar 

  42. 42

    Olofsson, H., Frame, A. M. & Servedio, M. R. Can reinforcement occur with a learned trait? Evolution 65, 1992–2003 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  43. 43

    Hudson, E. J. & Price, T. D. Pervasive reinforcement and the role of sexual selection in biological speciation. Heredity 105, 821–833 (2014).

    Article  Google Scholar 

  44. 44

    Wheatcroft, D. Reproductive interference via display signals: the challenge of multiple receivers. Pop. Ecol. 57, 333–337 (2015).

    Article  Google Scholar 

  45. 45

    Ellegren, H. et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756–760 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. 46

    Hauber, M. E., Russo, S. A. & Sherman, P. W. A password for species recognition in a brood-parasitic bird. Proc. R. Soc. Lond. B 268, 1041–1048 (2001).

    CAS  Article  Google Scholar 

  47. 47

    Davies, N. B., Madden, J. R. & Butchart, S. H. Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species. Proc. R. Soc. Lond. B 271, 2297–2304 (2004).

    CAS  Article  Google Scholar 

  48. 48

    Wheatcroft, D. Repetition rate of calls used in multiple contexts communicates presence of predators to nestlings and adult birds. Anim. Behav. 103, 35–44 (2015).

    Article  Google Scholar 

  49. 49

    Long, K. D., Kennedy, G. & Balaban, E. Transferring an inborn auditory perceptual predisposition with interspecies brain transplants. Proc. Natl Acad. Sci. USA 98, 5862–5867 (2001).

    CAS  PubMed  Article  Google Scholar 

  50. 50

    Wheatcroft, D. & Qvarnström, A. A blueprint for vocal learning: auditory predispositions from brains to genomes. Biol. Lett. 11, 20150155 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  51. 51

    Qvarnström, A., Wiley, C., Svedin, N. & Vallin, N. Life-history divergence facilitates regional coexistence of competing Ficedula flycatchers. Ecology 90, 1948–1957 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  52. 52

    Rybinski, J. et al. Competition-driven build-up of habitat isolation and selection favoring modified dispersal patterns in a young avian hybrid zone. Evolution 70, 2226–2238 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  53. 53

    Epsmark, Y. O. & Lampe, H. M. Variations in the song of the pied flycatcher within and between breeding seasons. Bioacoustics 5, 33–65 (1993).

    Article  Google Scholar 

  54. 54

    Svedin, N., Wiley, C., Veen, T., Gustafsson, L. & Qvarnström, A. Natural and sexual selection against hybrid flycatchers. Proc. R. Soc. Lond. B 375, 735–744 (2008).

    Article  Google Scholar 

  55. 55

    Ålund, M., Immler, S., Rice, A. M. & Qvarnström, A. Low fertility of wild hybrid male flycatchers despite recent divergence. Biol. Lett. 9, 20130169 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  56. 56

    Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. 57

    Bioacoustics Research Program. Raven pro: Interactive Sound Analysis Software (The Cornell Lab of Ornithology, 2008).

  58. 58

    Cramer, H. Mathematical Methods of Statistics (Princeton Univ. Press, 1946).

    Google Scholar 

  59. 59

    Wilson, V. L. Critical values of the rank-biserial correlation coefficient. Educ. Psychol. Meas. 36, 297–300 (1976).

    Article  Google Scholar 

  60. 60

    Bates, D., Maecher, M., Bolker, B. M. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Soft. 67, 1–48 (2015).

  61. 61

    R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).

  62. 62

    Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Soft. 69, 1–33 (2016).

    Article  Google Scholar 

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We thank T. Price, D. Shizuka and T. Suzuki for invaluable comments and discussions on the manuscript, and R. Dufva for laboratory assistance. D.W. was funded by the National Science Foundation (award ID: 1202861;, the Nilsson-Ehle Endowment ( and the Stiftelsen för Zoologisk Forskning (Uppsala University). A.Q. was funded by the Swedish Research Council ( and the Royal Swedish Academy of Sciences (

Author information




D.W. conceived of and designed the study, contributed materials, conducted the experiments, analysed the data and wrote the manuscript. A.Q. designed the study, contributed materials and wrote the manuscript.

Corresponding author

Correspondence to David Wheatcroft.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1 and 2; Supplementary Tables 1–10 (PDF 652 kb)

Supplementary Table 11

Song recordings used for each experiment. (CSV 1 kb)

Supplementary Table 12

Raw behavioural measurements. (CSV 150 kb)

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Wheatcroft, D., Qvarnström, A. Genetic divergence of early song discrimination between two young songbird species. Nat Ecol Evol 1, 0192 (2017).

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