A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird

• Authors: Jennifer R. Merritt, Emory University; Kathleen E. Grogan, Emory University; Wendy Zinzow-Kramer, Emory University; Dan Sun, Georgia Institute of Technology; Eric Ortlund, Emory University; Soojin V. Yi, Georgia Institute of Technology; Donna Maney, Emory University
• Journal Title: Proceedings of the National Academy of Sciences of the United States of America
• Volume: Volume 117, Number 35
• Publisher: National Academy of Sciences | 2020-09-01, Pages 21673-21680
• Type of Work: Article | Final Publisher PDF
• Publisher DOI: http://doi.org/10.1073/pnas.2011347117
• Subjects: Biology, Genetics; Chemistry, Biochemistry; Psychology, Psychobiology
• Keywords: Science & Technology; Multidisciplinary Sciences; Science & Technology - Other Topics; chromosomal inversion; songbird; social behavior; White throated sparrow; Zonotrichia albicollis; Gene disruption; Trade-offs; Life; Alpha; Evolution; Organization; Architecture

Abstract

Behavioral evolution relies on genetic changes, yet few behaviors can be traced to specific genetic sequences in vertebrates. Here we provide experimental evidence showing that differentiation of a single gene has contributed to the evolution of divergent behavioral phenotypes in the white-throated sparrow, a common backyard songbird. In this species, a series of chromosomal inversions has formed a supergene that segregates with an aggressive phenotype. The supergene has captured ESR1, the gene that encodes estrogen receptor α (ERα); as a result, this gene is accumulating changes that now distinguish the supergene allele from the standard allele. Our results show that in birds of the more aggressive phenotype, ERα knockdown caused a phenotypic change to that of the less aggressive phenotype. We next showed that in a freeliving population, aggression is predicted by allelic imbalance favoring the supergene allele. Finally, we identified cis-regulatory features, both genetic and epigenetic, that explain the allelic imbalance. This work provides a rare illustration of how genotypic divergence has led to behavioral phenotypic divergence in a vertebrate.