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Repeated behavioural evolution is associated with convergence of gene expression in cavity-nesting songbirds

Nature Ecology & Evolution volume 9, pages 845–856 (2025)Cite this article

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Abstract

Uncovering the genomic bases of phenotypic adaptation is a major goal in biology, but this has been hard to achieve for complex behavioural traits. Here we leverage the repeated, independent evolution of obligate cavity nesting in birds to test the hypothesis that pressure to compete for a limited breeding resource has facilitated convergent evolution in behaviour, hormones and gene expression. We used an integrative approach, combining aggression assays in the field, testosterone measures and transcriptome-wide analyses of the brain in wild-captured females and males. Our experimental design compared species pairs across five avian families, each including one obligate cavity-nesting species and a related species with a more flexible nest strategy. We find behavioural convergence, with higher levels of territorial aggression in obligate cavity nesters, particularly among females. Across species, levels of testosterone in circulation were not associated with nest strategy nor aggression. Phylogenetic analyses of individual genes and co-regulated gene networks revealed more shared patterns of brain gene expression than expected by drift, although the scope of convergent gene expression evolution was limited to a small percentage of the genome. When comparing our results to other studies that did not use phylogenetic methods, we suggest that accounting for shared evolutionary history may reduce the number of genes inferred as convergently evolving. Altogether, we find that behavioural convergence in response to shared ecological pressures is associated with largely independent evolution of gene expression across different avian families, punctuated by a narrow set of convergently evolving genes.

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Fig. 1: Obligate cavity nesters displayed more overt territorial aggression.
Fig. 2: Concordance in differential expression based on RRHO.
Fig. 3: Tan4 gene network associated with obligate cavity nesting.
Fig. 4: Gene networks associated with female aggression.

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Data availability

The data that support the findings of this study are available in the Supplementary Information, on Github via Zenodo at https://doi.org/10.5281/zenodo.14715061 (ref. 86), and via Figshare repository at https://doi.org/10.6084/m9.figshare.26367061 (ref. 87). Raw sequence reads and count data can be obtained from the Gene Expression Omnibus database (GEO accession number GSE244480).

Code availability

Scripts for processing and analysing data are available on Github via Zenodo at https://doi.org/10.5281/zenodo.14715061 (ref. 86).

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Acknowledgements

For facilitating fieldwork, we thank the Indiana Department of Natural Resources; Indiana University’s Research and Teaching Preserve; T. Rothfus and C. Hagie at Therkilsden Field station; A. Fournier and S. Havera at Forbes Field Station; and J. Hoover, N. Antonson, H. Scharf and A. Funk. For vocal stimuli, we thank M. Wilkins, D. Reichard, C. Krieg and E. Chen. Thanks to E. Mueller for help with 3D printing; S. Nallu and J. Huang for TapeStation and library preparation; E. D. Curole and J. K. for assistance in the lab; and B. Young for assistance with data analysis. This work was funded by the US National Science Foundation grant DBI-1907134 (S.E.L.), DBI-2146866 (M.W.H.), IOS-1953226 (M.E.H.) and CAREER grant IOS-1942192 (K.A.R.), as well as support from Indiana University Biology, Loyola Biology and Duke Biology.

Author information

Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington, IN, USA

    Sara E. Lipshutz, Mark S. Hibbins, Alexandra B. Bentz, Tara A. Empson, Elizabeth M. George, Samuel J. Torneo, Abbigail M. Turner, Sarah E. Wolf, Mary J. Woodruff, Matthew W. Hahn & Kimberly A. Rosvall

  2. Department of Biology, Loyola University Chicago, Chicago, IL, USA

    Sara E. Lipshutz & Quinn K. Thomas

  3. Department of Biology, Duke University, Durham, NC, USA

    Sara E. Lipshutz

  4. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada

    Mark S. Hibbins

  5. School of Biological Sciences, University of Oklahoma, Norman, OK, USA

    Alexandra B. Bentz

  6. Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN, USA

    Aaron M. Buechlein & Douglas B. Rusch

  7. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA

    Tara A. Empson

  8. Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH, USA

    Elizabeth M. George

  9. Department of Evolution, Ecology, and Behavior, University of Illinois Urbana-Champaign, Urbana, IL, USA

    Mark E. Hauber, Wendy M. Schelsky & Abbigail M. Turner

  10. Illinois Natural History Survey, Prairie Research Institute, University of Illinois Urbana-Champaign, Champaign, IL, USA

    Mark E. Hauber & Wendy M. Schelsky

  11. Advanced Science Research Center and Programs in Biology and in Psychology, Graduate Center of the City University of New York, New York, NY, USA

    Mark E. Hauber

  12. The Grainger College of Engineering, University of Illinois Urbana-Champaign, Urbana, IL, USA

    Wendy M. Schelsky

  13. School of Biological Sciences, University of Edinburgh, Edinburgh, Scotland, UK

    Sarah E. Wolf

  14. United States Department of Agriculture, Animal and Plant Health Inspection Services, Veterinary Services, Center for Epidemiology and Animal Health, Fort Collins, CO, USA

    Mary J. Woodruff

  15. Department of Computer Science, Indiana University, Bloomington, IN, USA

    Matthew W. Hahn

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  1. Sara E. Lipshutz
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  2. Mark S. Hibbins
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  16. Kimberly A. Rosvall
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Contributions

S.E.L. and K.A.R. conceived of the study; S.E.L. led the data collection, supported by A.B.B., A.M.T., E.M.G, M.E.H., M.J.W., S.J.T, S.E.W., T.A.E. and W.M.S.; S.E.L., M.S.H., A.B.B., A.M.B., D.B.R., Q.K.T., M.W.H. and K.A.R. analysed and interpreted the data; S.E.L., M.S.H. and K.A.R. wrote the paper, and all authors contributed to revisions. The manuscript reflects the contributions and ideas of all authors.

Corresponding authors

Correspondence to Sara E. Lipshutz or Kimberly A. Rosvall.

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Lipshutz, S.E., Hibbins, M.S., Bentz, A.B. et al. Repeated behavioural evolution is associated with convergence of gene expression in cavity-nesting songbirds. Nat Ecol Evol 9, 845–856 (2025). https://doi.org/10.1038/s41559-025-02675-x

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