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).

  2. 2

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

  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).

  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).

  5. 5

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

  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).

  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).

  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).

  9. 9

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

  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).

  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).

  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).

  13. 13

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

  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).

  15. 15

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

  16. 16

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

  17. 17

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

  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).

  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).

  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).

  21. 21

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

  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).

  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).

  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).

  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).

  27. 27

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

  28. 28

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

  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).

  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).

  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).

  32. 32

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

  33. 33

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

  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).

  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).

  36. 36

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

  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).

  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).

  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).

  40. 40

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

  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).

  42. 42

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

  43. 43

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

  44. 44

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

  45. 45

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

  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).

  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).

  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).

  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).

  50. 50

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

  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).

  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).

  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).

  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).

  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).

  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).

  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).

  59. 59

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

  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).

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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.

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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