Genes located in a chromosomal inversion are correlated with territorial song in white‐throated sparrows

The genome of the white‐throated sparrow (Zonotrichia albicollis) contains an inversion polymorphism on chromosome 2 that is linked to predictable variation in a suite of phenotypic traits including plumage color, aggression and parental behavior. Differences in gene expression between the two color morphs, which represent the two common inversion genotypes (ZAL2/ZAL2 and ZAL2/ZAL2m), may therefore advance our understanding of the molecular underpinnings of these phenotypes. To identify genes that are differentially expressed between the two morphs and correlated with behavior, we quantified gene expression and terrirorial aggression, including song, in a population of free‐living white‐throated sparrows. We analyzed gene expression in two brain regions, the medial amygdala (MeA) and hypothalamus. Both regions are part of a ‘social behavior network’, which is rich in steroid hormone receptors and previously linked with territorial behavior. Using weighted gene co‐expression network analyses, we identified modules of genes that were correlated with both morph and singing behavior. The majority of these genes were located within the inversion, showing the profound effect of the inversion on the expression of genes captured by the rearrangement. These modules were enriched with genes related to retinoic acid signaling and basic cellular functioning. In the MeA, the most prominent pathways were those related to steroid hormone receptor activity. Within these pathways, the only gene encoding such a receptor was ESR1 (estrogen receptor 1), a gene previously shown to predict song rate in this species. The set of candidate genes we identified may mediate the effects of a chromosomal inversion on territorial behavior. Weighted gene co‐expression network analysis was used to create gene expression networks for two brain regions relevant for social behavior: medial amygdala (MeA) and hypothalamus (HYP). Within each network, one module* (group of co‐expressed genes) was enriched in genes captured by a chromosomal rearrangement and correlated with plumage morph (morph) and song rate (songs). The color bar at top indicates the module to which each gene was assigned. In the second row, genes located on chromosome 2 (Chr2) are indicated by black bars. The majority of genes located on Chr2 are captured by a chromosomal rearrangement. Colored bars in rows 3–6 indicate gene significance (GS): the correlation between gene expression and the indicated trait or gene. Red indica