The generation of species-specific singing in songbirds is associated with species-specific patterns of gene activity in brain regions called song nuclei, according to a study published November 12 in the open-access journal PLOS Biology by Kazuhiro Wada of Hokkaido University in Japan, and colleagues. According to the authors, the findings could be a promising step toward a better understanding of the contribution of multiple genes to the evolution of behaviors.
Learning of most complex motor skills, such as birdsong and human speech, is constrained in a manner that is characteristic of each species, but the mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is also thought to depend on species-specific patterns of gene activity in song nuclei — brain regions known to be specialized for vocal learning and production.
In the new study, Wada and colleagues made use of two closely related songbird species — the zebra finch (Taeniopygia guttata) and the owl finch (Taeniopygia bichenovii) — and also the hybrid offspring of matings between these two species. This allowed them to examine the relationship between inter-species differences in gene expression and the production of species-specific song patterns.
The researchers compared the songs of birds that had been taught the same species’ song versus those that had only heard the other species’ song; this showed that the song learning was mostly regulated by species-specific genetic differences. They then identified genes whose activity in song nuclei is regulated in a species-specific fashion, either by changes in the genes’ own regulatory regions (“cis-regulation”) or by changes in other proteins that affect a gene’s activity (“trans-regulation”).
They found that trans-regulatory changes were more prevalent than cis-regulatory changes and tended to primarily affect the activity of genes involved in the formation of nerve connections and transmission of information between neurons in one particular song nucleus, “RA” — considered as birds’ counterpart to the mammalian laryngeal motor cortex.
They identified a signaling molecule called BDNF as a mediator of changes in trans-regulated of genes in RA, with a significant correlation between individual variation in the amount of BDNF and species-specific song properties. This was supported by the fact that the use of a drug to over-activate BDNF receptors altered the activity of trans-regulated genes in the RA and disrupted the structures of learned songs in the adult zebra finch.
These results demonstrate functional neurogenetic associations between inter-species differences in gene regulation and species-specific learned behaviors. According to the authors, future research building on these findings could reveal the specific gene regulatory changes that underlie the evolution of species-specific learned behaviors.
“We believe that this isn’t just about bird songs,” the lead author, Kazuhiro Wada said. “Our study is a promising step to understand how the changes in gene regulation could eventually lead to the evolution of species-specific animal behaviors.”
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Citation: Wang H, Sawai A, Toji N, Sugioka R, Shibata Y, Suzuki Y, et al. (2019) Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds. PLoS Biol 17(11): e3000476. https://doi.org/10.1371/
Funding: This work was supported by a Japanese MEXT scholarship and the China Scholarship Council (CSC#201408210091) to HW, MEXT/JSPS KAKENHI Grant Number #4903-JP17H06380, JP17H05932, JP17K19629, and JP18H02520 to KW, and RNA-seq experiments were supported by MEXT KAKENHI 221S0002. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
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