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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 free-living 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.

Citation

Jennifer R Merritt, Kathleen E Grogan, Wendy M Zinzow-Kramer, Dan Sun, Eric A Ortlund, Soojin V Yi, Donna L Maney. A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird. Proceedings of the National Academy of Sciences of the United States of America. 2020 Sep 01;117(35):21673-21680

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PMID: 32817554

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