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Phylotranscriptomics reveals the convergent evolution of aggression is associated with both shared and unique patterns of gene expression evolution in cavity nesting songbirds

ABSTRACT: Uncovering the genomic regulation 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 evolution of obligate cavity-nesting in birds to test the hypothesis that the shared pressure to compete for a limited breeding resource drives convergent behavioral evolution via convergent gene regulatory changes in the brain. Using behavioral assays in the field, hormonal measures, and transcriptome-wide analyses in 10 focal species, we examined females and males in five avian families, each including one obligate cavity-nesting species and a related species with a more flexible nesting strategy. Results support the hypothesis of behavioral convergence, with high levels of territorial aggression in obligate cavity-nesters, particularly among females. Levels of testosterone were not associated with nesting strategy for either sex, but phylogenetic analyses of individual genes and co-regulated gene networks revealed some shared patterns of gene expression, with functional enrichment related to metabolic and mitochondrial processes. Though this gene regulatory convergence may contribute to behavioral convergence, concordance in gene expression did not scale across multiple families. These observations indicate that replicated evolutionary increases in aggression arise via largely lineage-specific changes in brain gene expression.

ORGANISM(S): Sialia sialis Passer montanus Passer domesticus Setophaga petechia Thryothorus ludovicianus Tachycineta bicolor Hirundo rustica Turdus migratorius Troglodytes aedon Protonotaria citrea

PROVIDER: GSE244480 | GEO | 2025/04/29

REPOSITORIES: GEO

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Project description:Animal and human studies suggest that inflammation is associated with behavioral disorders including aggression. We have recently shown that physical aggression of boys during childhood is strongly associated with reduced plasma levels of cytokines IL-1a, IL-4, IL-6, IL-8 and IL-10, later in early adulthood (Provencal et al., unpublished data). This study tests the hypothesis that there is an association between differential DNA methylation regions in cytokine genes in T cells and monocytes DNA in adult subjects and a trajectory of physical aggression from childhood to adolescence. We compared the methylation profiles of the entire genomic loci encompassing the IL-1a, IL-6, IL-4, IL10 and IL8 and three of their regulatory transcription factors (TF) NFkB1, NFAT5 and STAT6 genes in adult males on a chronic physical aggression trajectory (CPA) and males with the same background who followed a normal physical aggression trajectory (control group). We used the method of methylated DNA immunoprecipitation (MeDIP) with comprehensive cytokine gene loci and TF loci microarray hybridization, statistical analysis and false discovery rate correction. We recruited two groups of Caucasian males who were born in families with a low socioeconomic status and were living at the time of the present study within 200km from our laboratory. The first group, composed of 8 subjects, had a history of chronic physical aggression from age 6 to 15 years (chronic physical aggression group, CPA). The second group, composed of 12 subjects, was recruited from the same longitudinal studies but included only those who did not have a history of chronic physical aggression from age 6 to 15 (Control group, CG). Using custom-designed microarrays with 44K probes tiling cytokines IL-1a, IL-6, IL-4, IL10 and IL8 and three of their regulatory transcription factors (TF) NFkB1, NFAT5 and STAT6, we obtained DNA methylation profiles by meDIP-chip. Each profile was generated in triplicate.

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Phylotranscriptomics reveals the convergent evolution of aggression is associated with both shared and unique patterns of gene expression evolution in cavity nesting songbirds

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