To Tame a Songbird: 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 BF 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 overall augmented aggression and stress responses.

Fig. 1.

The WBM (left; wild; blue) and the BF (right; domesticated; green).(A) Environmental variables and their relationship with stress and birdsong complexity in the wild and domesticated scenarios. (B) PCA of whole genomic genotype likelihoods in WBM and BF. (C) BF and WBM unfolded Site Frequency Spectrums.

Fig. 2.

Genetic differentiation and variability in WBM (wild; blue) and BF (domesticated; green) populations. (top to bottom) Schematic representation of defined ROIs enclosing sweep signals discussed in this study; 10kb window measures of differentiation between the two populations, calculated as the averaged Fst across all positions within the window; 10kb window estimations of nucleotide diversity, calculated as the Tajima’s D (TajD), Waterson’s theta (tW) and Pairwise theta (tW) across all positions within the window.

Fig. 3.

Selection signals in WBM (wild; blue) and BF (domesticated; green) populations. (top to bottom) Schematic representation of defined ROIs enclosing sweep signals discussed in this study; selection signals in WBM and BF populations. Each data point represents a window’s composite likelihood of a selective sweep (CLR). Labels highlight the genes within ROIs referred to in the main text.