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 constraints, presumably of genetic origin. A celebrated, if contentious, example is whether a universal grammar constrains syntactic diversity in human languages. Oscine songbirds exhibit song learning and provide biologically tractable models of culture: members of a species show individual variation in song and geographically separated groups have local song dialects. Different species exhibit distinct song cultures, suggestive of genetic constraints. Without such constraints, innovations and copying errors should cause unbounded variation over multiple generations or geographical distance, contrary to observations. 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 required. Zebra finch isolates, unexposed to singing males during development, produce song with characteristics that differ from the wild-type song found in laboratory 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 evolution. In analogy to models in quantitative genetics, 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.

Figure 1. Wild-type songs versus isolate songs

a, Spectral derivatives of two WT song bouts. Different syllable types are underlined in different colors. Syllables show stereotypical organization into song motifs and rapid acoustic transitions within syllables. b, Isolate song bouts. Some syllables are extremely long (Bird 4, yellow) and others are stuttered (Bird 3, yellow and blue). c, Mean distribution histogram of frequency modulation in WT birds (blue, n=52) versus ISO birds (red, n=17). Dotted lines represent 95% confidence intervals. d, Histogram of duration of acoustic state, demonstrating longer durations in ISO. e, Spectra of rhythm frequencies showing less structured rhythm in ISO. The dotted gray line marks the minimum frequency that we used for further analysis (0.5 Hz).

Figure 2. Progression toward WT song in pupils of isolates

First two PCs constructed from a, spectral features; b, DAS; c, rhythm frequencies. Dots represent individual WT (blue, n=52) and ISO (red, n=17) birds. Bayes classification lines are shown in gray. Histogram (bottom) of PC1 in first-generation (black, n=13) pupils falls between WT and ISO. d–f, Same data as in ac. Arrows originate at the tutors and point toward pupils. Different colors represent different tutors. Purple shading indicates center of WT cluster. Numerals indicate the arrows corresponding to the songs in g and i. g–h, Biased copying of syllable durations. i, Biased copying of syllable abundance and emergence of song motif. Shaded rectangle: overlay of syllable B and its imitation, B′. j, Correlation between first PCs of pupil versus tutor, indicating biased imitation. Dashed red line represents 95% confidence band, and the dashed blue line is the identity line.

Figure 3. Multi-generational progression toward WT song

a, Schematic diagram of the experimental paradigm. Pupils become tutors when they reach adulthood (day 120–140). b, Three examples of the songs of isolate tutors and the succeeding generations of learners. Blue and red boxes show individual syllable types that are altered by pupils. Long, monotonic syllables become shorter and more differentiated (left and right panels). Rarely, syllables were omitted (middle panel) in later generations of learners c–e, PCA of song features, state duration and rhythm spectra. As in Fig. 2d–f, arrows originate at the tutors and point toward pupils. The progression toward the WT cloud (purple ovals) continues over generations.

Figure 4. Progression toward WT song in an isolated colony

a, Family relationships in the first 5 clutches based on behavioral observations. b–d, PCA of song features, state duration and rhythm (as in Fig. 2d–f). The colony founder is marked by red dot. Colors and symbols identify individuals in (a). Successive clutches approach the WT cloud (purple shading) in the song features, especially in rhythm frequencies. e, A long syllable that dominates the founder isolate song motif, and its imitations in successive clutches.