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Author Notes:

Email: dmaney@emory.edu or soojinyi@gatech.edu.

Author contributions: D.S., D.L.M., and S.V.Y. designed research; D.S., I.H., W.M.Z.-K., D.L.M., and S.V.Y. performed research; D.L.M. and S.V.Y. contributed new reagents/analytic tools; D.S., I.H., D.L.M., and S.V.Y. analyzed data; and D.S., D.L.M., and S.V.Y. wrote the paper.

We thank the Roy Carver Genome Center of the University of Illinois for help with sequencing; Dr. Kathleen Grogan, members of the S.V.Y. laboratory, Brian Charlesworth, and two anonymous reviewers for comments on the manuscript; and Xiulan Pan and Chen Feng for help with illustration.

The authors declare no conflict of interest.


Research Funding:

This work was supported by National Institutes of Health Grants R01 MH082833 (to D.L.M.) and 1R21 NIMH102677 (to D.L.M. and S.V.Y.) and by Georgia Tech (S.V.Y.).


  • suppression of recombination
  • genetic degeneration
  • regulatory evolution
  • dosage compensation
  • sex chromosomes

Rapid regulatory evolution of a nonrecombining autosome linked to divergent behavioral phenotypes


Journal Title:

Proceedings of the National Academy of Sciences


Volume 115, Number 11


, Pages 2794-2799

Type of Work:

Article | Final Publisher PDF


In the white-throated sparrow (Zonotrichia albicollis), the second chromosome bears a striking resemblance to sex chromosomes. First, within each breeding pair of birds, one bird is homozygous for the standard arrangement of the chromosome (ZAL2/ZAL2) and its mate is heterozygous for a different version (ZAL2/ZAL2 m ). Second, recombination is profoundly suppressed between the two versions, leading to genetic differentiation between them. Third, the ZAL2 m version is linked with phenotypic traits, such as bright plumage, high aggression, and low parental behavior, which are usually associated with males. These similarities to sex chromosomes suggest that the evolutionary mechanisms that shape sex chromosomes, in particular genetic degeneration of the heterogametic version due to the suppression of recombination, are likely important in this system as well. Here, we investigated patterns of protein sequence evolution and gene expression evolution between the ZAL2 and ZAL2 m chromosomes by whole-genome sequencing and transcriptome analyses. Patterns of protein evolution exhibited only weak signals of genetic degeneration, and few genes harbored signatures of positive selection. We found substantial evidence of transcriptome evolution, such as significant expression divergence between ZAL2 and ZAL2 m alleles and signatures of dosage compensation for highly expressed genes. These results suggest that, early in the evolution of heteromorphic chromosomes, gene expression divergence and dosage compensation can prevail before large-scale genetic degeneration. Our results show further that suppression of recombination between heteromorphic chromosomes can lead to the evolution of alternative (sex-like) behavioral phenotypes before substantial genetic degeneration.

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© 2018 National Academy of Sciences. All Rights Reserved.

This is an Open Access work distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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