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Abstract Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host’s egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts. 

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. 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 behavioral 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, but the scope of convergent gene expression evolution was limited to a small percent 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 behavioral convergence in response to shared ecological pressures is associated with largely independent gene expression evolution across different avian families, punctuated by a narrow set of convergently evolving genes.