Mismatch in sexual dimorphism of developing song and song control system in blue-capped cordon-bleus, a songbird species with singing females and males

Muriele Lobato,Christoph Gahr,Nicole Geberzahn,Manfred Gahr,Albertine Leitão,Michiel Vellema,Silene M A De Lima

doi:10.3389/fevo.2015.00117

Abstract

Brain song control regions of adult passerine birds are sexually dimorphic in species such as the zebra finch (Taeniopygia guttata) in which males sing whereas females do not. In many tropical bird species, however, females sing as well. Here we study for the first time the ontogeny of the song control system and the song in a species, in which both male and female sing regularly. In blue-capped cordon-bleus (Uraeginthus cyanocephalus), a distant relative of the zebra finch, both males and females start singing at around 30-40 day post-hatching (dph). First we quantified that sex-specific differences in song features emerged only in adulthood, after 250 dph of age: Adult females sang complex songs, which were slightly shorter and contained fewer syllables as compared to the males. Second, the development of forebrain song control regions HVC (proper name) and RA (nucleus robustus arcopallii) of blue-capped cordon-bleus was quantified in both sexes at 20, 30, 50, 100, 150, 250 dph as well as in old adults. The volume and neuron numbers of the HVC and RA were sexually dimorphic throughout the entire development and remained sexually dimorphic in adulthood. Since singing developed in a non sex-specific way until 250 dph, neural sex differences to a large extend precede the behavioral (song) sex differences. This suggests that these neuroanatomical sex differences are not causally related to the sexual differentiation of song patterns in this species.

Highlights

A frequently used argument to suggest that female songbirds are not capable of singing or sing only simple songs is that the neuroanatomy of the forebrain song control areas is sexually dimorphic (Nottebohm and Arnold, 1976; DeVoogd and Nottebohm, 1981; Brenowitz and Arnold, 1986; DeVoogd et al, 1993; Gahr et al, 1998; MacDougall-Shackelton and Ball, 1999)
The prime example of this sexual dimorphism of the song control system and singing is the zebra finch, in which stark neuroanatomical sex differences correlate with the lack of singing of adult females (Nottebohm and Arnold, 1976), even after testosterone treatment, a paradigm that induces singing in males of all species tested
It was thought that females of only some species sing (e.g., Beletsky, 1983; Gahr and Güttinger, 1985; Hoelzel, 1986; Langmore et al, 1996; Yamaguchi, 2001). One reason for this discrepancy might be that song system development was never studied in a species in which females sing regularly. We studied both the song system development and the song development in a songbird species, the blue-capped cordon-blue (Uraeginthus cyanocephalus) in which males and females sing frequently both during ontogeny and in adulthood (Geberzahn and Gahr, 2011, 2013)

Summary

Introduction

A frequently used argument to suggest that female songbirds are not capable of singing or sing only simple songs is that the neuroanatomy of the forebrain song control areas (collectively called the song system) is sexually dimorphic (Nottebohm and Arnold, 1976; DeVoogd and Nottebohm, 1981; Brenowitz and Arnold, 1986; DeVoogd et al, 1993; Gahr et al, 1998; MacDougall-Shackelton and Ball, 1999). The prime example of this sexual dimorphism of the song control system and singing is the zebra finch, in which stark neuroanatomical sex differences correlate with the lack of singing of adult females (Nottebohm and Arnold, 1976), even after testosterone treatment, a paradigm that induces singing in males of all species tested (for review Gahr, 2014). This neuroanatomical sex-difference of zebra finches emerges during ontogeny due to genetic and endocrine mechanisms (Gurney and Konishi, 1980; Wade and Arnold, 1996; Gahr and Metzdorf, 1999; Holloway and Clayton, 2001; Agate et al, 2003). This potential to sing correlates with the differentiation of their song control areas, which is relatively smaller as compared to canary males but relatively larger as compared to female zebra finches (Nottebohm and Arnold, 1976; Nottebohm, 1980)

Methods

Results

Conclusion