Phylotranscriptomics reveals convergent behavioral evolution associated with shared and unique mechanisms in cavity-nesting songbirds

Abstract

Uncovering the genomic bases of phenotypic adaptation is a major goal in biology, but this has been hard to achieve for complex behavioral 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 behavior, hormones, and gene expression. Using aggression assays in the field, testosterone measures, and transcriptome-wide analyses of the brain in wild-captured females and males, we examined 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 behavioral convergence, with higher levels of territorial aggression in obligate cavity-nesters, particularly among females. Levels of testosterone in circulation were not associated with nest strategy, nor aggression. Phylogenetic analyses of individual genes and co-regulated gene networks revealed shared patterns of brain gene expression, but the scope of convergent gene expression evolution was limited to a small percent of the genome. Together, these observations indicate that replicated evolutionary changes in aggression arise via a combination of both repeated and independent evolution of gene regulation.