Abstract

It is thought that neural sex differences are functionally related to sex differences in the behaviour of vertebrates. A prominent example is the song control system of songbirds. Inter-specific comparisons have led to the hypothesis that sex differences in song nuclei size correlate with sex differences in song behaviour. However, only few species with similar song behaviour in both sexes have been investigated and not all data fit the hypothesis. We investigated the proposed structure – function relationship in a cooperatively breeding and duetting songbird, the white-browed sparrow weaver (Plocepasser mahali). This species lives in groups of 2–10 individuals, with a dominant breeding pair and male and female subordinates. While all male and female group members sing duet and chorus song, a male, once it has reached the dominant position in the group, sings an additional type of song that comprises a distinct and large syllable repertoire. Here we show for both types of male – female comparisons a male-biased sex difference in neuroanatomy of areas of the song production pathway (HVC and RA) that does not correlate with the observed polymorphism in song behaviour. In contrast, in situ hybridisation of mRNA of selected genes expressed in the song nucleus HVC reveals a gene expression pattern that is either similar between sexes in female – subordinate male comparisons or female-biased in female – dominant male comparisons. Thus, the polymorphic gene expression pattern would fit the sex- and status-related song behaviour. However, this implies that once a male has become dominant it produces the duetting song with a different neural phenotype than subordinate males.

Highlights

  • Sex differences in brain structure and behaviour are widespread among vertebrates

  • Besides the analysis of overall song system neuroanatomy, we focused on possible sex differences in expression levels of selected genes in the major song nucleus HVC

  • We report that in a duetting songbird with a complex social system, the extent of sex differences within the song control system varies according to the males’ dominance rank

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Summary

Introduction

Sex differences in brain structure and behaviour are widespread among vertebrates. In mammals, including humans, numerous studies have accumulated evidence for sex differences in brain anatomy, neurochemistry and activity. In contrast to most mammalian neural circuits with sex differences, the song control system of songbirds is a functionally well-defined neural circuit that has become a widely-used model for the study of brainbehaviour relationships (for review, [4]). This network of forebrain areas, responsible for song learning and song production, was found to exhibit extreme sex differences in size and neuron number in some species [5]. In bay wrens (Thryothorus nigricapillus), a duetting species with similar song in males and females, RA, HVC and area X are only about 1.1–1.5 times larger in males compared to females [6] These anatomical sex differences are thought to be functionally related to sex differences in vocal behaviour. Findings from two duetting songbird species with monomorphic singing, provide evidence that similar song performance in males and females does not necessitate similar neural gross morphology [10,11]

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