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

Fehér O, Wang H, Saar S, Mitra PP, Tchernichovski O - Nature (2009)

Bottom Line: 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.Consequently, songs evolved towards the wild-type in three to four generations.Our study has parallels with language change and evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, City College, City University of New York, New York 10031, USA. olcifeher@gmail.com

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.

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Progression toward WT song in an isolated colonya, 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.
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Figure 4: Progression toward WT song in an isolated colonya, 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.

Mentions: In this social situation, too, the isolate colony approached the WT cluster over a few generations (Fig. 4). To judge the transition toward WT clusters, we examined PC projections with the isolate tutor song marked as a red dot. Comparing the trajectory shown in Fig. 4e to that of Fig. 3b, right panel (originating from the same tutor), we see that the outcome in the colony is similar to that observed in one-to-one tutoring. Even though the outcome of the colony experiment can only be judged qualitatively, we find it remarkable that despite intense social interactions, female presence and mating competition, there were only mild differences between birds in the two conditions. In the colony, juveniles also imitated sibling syllables and female long calls, leading to more complex songs (Supplementary 1c). In contrast to one-to-one tutoring, the best progress toward WT song occurred in rhythm, perhaps because birds incorporated additional syllable types into their song motifs.


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

Fehér O, Wang H, Saar S, Mitra PP, Tchernichovski O - Nature (2009)

Progression toward WT song in an isolated colonya, 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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2693086&req=5

Figure 4: Progression toward WT song in an isolated colonya, 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.
Mentions: In this social situation, too, the isolate colony approached the WT cluster over a few generations (Fig. 4). To judge the transition toward WT clusters, we examined PC projections with the isolate tutor song marked as a red dot. Comparing the trajectory shown in Fig. 4e to that of Fig. 3b, right panel (originating from the same tutor), we see that the outcome in the colony is similar to that observed in one-to-one tutoring. Even though the outcome of the colony experiment can only be judged qualitatively, we find it remarkable that despite intense social interactions, female presence and mating competition, there were only mild differences between birds in the two conditions. In the colony, juveniles also imitated sibling syllables and female long calls, leading to more complex songs (Supplementary 1c). In contrast to one-to-one tutoring, the best progress toward WT song occurred in rhythm, perhaps because birds incorporated additional syllable types into their song motifs.

Bottom Line: 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.Consequently, songs evolved towards the wild-type in three to four generations.Our study has parallels with language change and evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, City College, City University of New York, New York 10031, USA. olcifeher@gmail.com

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.

Show MeSH
Related in: MedlinePlus