The genomics of the domestication syndrome in a songbird model species

Abstract

Many domesticated animals share a syndromic phenotype marked by a suite of traits that include more variable patterns of coloration, reduced stress, aggression, and altered risk-taking and exploratory behaviors relative to their wild counterparts. Roughly 150 years after Darwin's pioneering insight into this phenomenon, reasonable progress has been made in understanding the evolutionary and biological basis of the so-called domesticated phenotype in mammals. However, the extent to which these processes are paralleled in non-mammalian domesticates is scant. Here, we address this knowledge gap by investigating the genetic basis of the domesticated phenotype in the Bengalese finch, a songbird frequently found in pet shops and a popular animal model in the study of learned vocal behaviors. Using whole-genome sequencing and population genomic approaches, we identify strain-specific selection signals in the Bengalee finch and its wild munia ancestor. Our findings suggest that, like in mammals, the evolution of the domestication syndrome in avian species involves a shift in the selective regime, capable of altering brain circuits favoring the dynamic modulation of motivation and reward sensitivity over augmented aggression and stress responses.

Fig. 1. Domestication drives behavioral and genomic divergence between Bengalese Finches and their wild ancestors, White-Rumped Munias.

BF (right; domesticated; green) and WRM (left; wild; blue). A Environmental variables and their relationship to stress and birdsong complexity in wild and domesticated scenarios. B PCA of whole genomic genotype likelihoods in BF and WRM. C BF and WRM unfolded Site Frequency Spectra. Photo credits: Maki Ikebuchi (Bengalese finch and white-rumped munia photographs) and Wikimedia Commons (world map).

Fig. 2. Genomic scans reveal putative domestication genes in Bengalese finches.

BF (domesticated; green) and WRM (wild; blue). Each panel brings a schematic representation of the genes (midpoint) annotated within the defined ROI, with genes discussed in the main text highlighted and labeled in red; 10 kb window-based measures of genetic differentiation (Fst) between BF and WRM populations, nucleotide diversity statistics (TajD, tW, and tP) for each BF and WBM populations; and CLR scores for a selective sweep for each BF and WBM populations. Yellow bars indicate gaps in the ZF reference genome. ROIs length is represented in Mb.

Fig. 3. Wild-specific selection signatures in White-Rumped Munias.

Plot structure and interpretation as in Fig. 2.