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De novo establishment of wild-type song culture in the zebra finch

Abstract

Culture is typically viewed as consisting of traits inherited epigenetically, through social learning. However, cultural diversity has species-typical constraints1, presumably of genetic origin. A celebrated, if contentious, example is whether a universal grammar constrains syntactic diversity in human languages2. Oscine songbirds exhibit song learning and provide biologically tractable models of culture: members of a species show individual variation in song3 and geographically separated groups have local song dialects4,5. Different species exhibit distinct song cultures6,7, suggestive of genetic constraints8,9. Without such constraints, innovations and copying errors should cause unbounded variation over multiple generations or geographical distance, contrary to observations9. Here we report an experiment designed to determine whether wild-type song culture might emerge over multiple generations in an isolated colony founded by isolates, and, if so, how this might happen and what type of social environment is required10. Zebra finch isolates, unexposed to singing males during development, produce song with characteristics that differ from the wild-type song found in laboratory11 or natural colonies. In tutoring lineages starting from isolate founders, we quantified alterations in song across tutoring generations in two social environments: tutor–pupil pairs in sound-isolated chambers and an isolated semi-natural colony. In both settings, juveniles imitated the isolate tutors but changed certain characteristics of the songs. These alterations accumulated over learning generations. Consequently, songs evolved towards the wild-type in three to four generations. Thus, species-typical song culture can appear de novo. Our study has parallels with language change and evolution12,13,14. In analogy to models in quantitative genetics15,16, we model song culture as a multigenerational phenotype partly encoded genetically in an isolate founding population, influenced by environmental variables and taking multiple generations to emerge.

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Figure 1: Wild-type songs versus isolate songs.
Figure 2: Progression towards WT song in pupils of isolates.
Figure 3: Multigenerational progression towards WT song.
Figure 4: Progression towards WT song in an isolated colony.

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Acknowledgements

We thank J. Wallman and H. Williams for critical reading of the manuscript and consultation and F. Nottebohm, C. Harding and N. Leader for recordings of WT songs. The study was supported by US National Institutes of Health (NIH) grants to O.T. and P.P.M., by a NIH Research Centers in Minority Institutions grant to City College, City University of New York, and by the Crick-Clay Professorship to P.P.M.

Author Contributions The idea for the study originated with P.P.M., with important modifications by O.T. and O.F. The experiments were carried out by O.F. and O.T. The model was developed by P.P.M. with help from H.W. All authors participated in the data analysis, with major efforts by H.W. and O.F.

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Correspondence to Olga Fehér.

Supplementary information

Supplementary Information 1

This file contains Supplementary Methods, Results and Statistical Analysis, Supplementary Figures 1-12 with Legends and Supplementary References. (PDF 2825 kb)

Supplementary Information 2

This file contains details of two theoretical models of interactions between tutors and pupils together with a review of background literature. (PDF 531 kb)

Supplementary Audio File

This file illustrates multi-generational song evolution. (WAV 9101 kb)

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Fehér, O., Wang, H., Saar, S. et al. De novo establishment of wild-type song culture in the zebra finch. Nature 459, 564–568 (2009). https://doi.org/10.1038/nature07994

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