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

Abstract

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), are therefore of potential interest toward understanding the molecular underpinnings of these phenotypes. To identify genes that are differentially expressed between the two morphs and correlated with behavior, we quantified both behavior and brain gene expression in a population of free-living white-throated sparrows. We quantified behavioral responses to simulated territorial intrusions (STIs) early during the breeding season. In the same birds, we then performed a transcriptome-wide analysis of gene expression in two regions, the medial amygdala 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 network analyses, we identified modules of genes that were correlated with both morph and STI-induced singing behavior. The majority of these genes were located within the inversion, demonstrating the profound effect the inversion has on the expression of genes captured by the rearrangement. Gene pathway analyses revealed that in the medial amygdala, 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 alpha). Our results thus suggest that ESR1 and related genes are important for behavioral differences between the morphs.

Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod

“…; Zinzow‐Kramer et al . ). Similarly, alternative reproductive strategies in the ruff ( Pliomachus pugnax ) were recently found to be controlled by polymorphic genes affecting sex hormone levels and plumage within an inversion that occurred about 3.8 million years ago (Küpper et al .…”

“…Putative adaptive genes within the inversions are indicated. Nishikawa et al 2015), and at least two inversions spanning about 100 Mb in white-throated sparrow (Zonotrichia albicollis) were shown to harbour genes associated with territorial song and plumage (Thomas et al 2008;Huynh et al 2011;Zinzow-Kramer et al 2015). Similarly, alternative reproductive strategies in the ruff (Pliomachus pugnax) were recently found to be controlled by polymorphic genes affecting sex hormone levels and plumage within an inversion that occurred about 3.8 million years ago (K€ upper et al 2015;Lamichhaney et al 2015).…”

Developmental stress and telomere dynamics in a genetically polymorphic species

“…White morph birds are heterozygous for an inversion‐based supergene on chromosome 2 (ZAL2 m /2), whereas tan morph birds are homozygous, lacking the rearrangement (ZAL2/2) (Thorneycroft, ; Tuttle et al., ). White birds are more aggressive, less parental and sing more than tan counterparts, and white males (WMs) are promiscuous (Knapton & Falls, ; Kopachena & Falls, ; Tuttle, ; Zinzow‐Kramer et al., ). Furthermore, white‐throated sparrows pair disassortatively by morph, producing a pair type with biparental care (tan males [TMs] × white females [WFs]; T × W), and a pair type with female‐biased care (WMs × tan females [TFs]; W × T) (Knapton & Falls, ; Tuttle, ).…”

Parent and offspring genotypes influence gene expression in early life

“…The light cyan module contains genes expressed at higher levels in W morph nestlings and contains eight hub genes, each located in the inversion (Table ). Three of these, EPM2A, BPNT1, and TAF5L, were also identified as hub genes in brain tissues of adult W morph males (Zinzow‐Kramer et al, ). These nestlings thus exhibit expression differences in inversion genes prior to any phenotypic or behavioural differences, revealing the importance of the inversion in maintaining morph phenotypes throughout life.…”