Species variation in the degree of sex differences in brain and behaviour related to birdsong: adaptations and constraints

Abstract

The song-control system, a neural circuit that controls the learning and production of birdsong, provided the first example in vertebrates of prominent macro-morphological sex differences in the brain. Forebrain nuclei HVC, robust nucleus of the arcopallium (RA) and area X all exhibit prominent male-biased sex differences in volume in zebra finches and canaries. Subsequent studies compared species that exhibited different degrees of a sex difference in song behaviour and revealed an overall positive correlation between male biases in song behaviour and male biases in the volume of the song nuclei. However, several exceptions have been described in which male biases in HVC and RA are observed even though song behaviour is equal or even female-biased. Other phenotypic measures exhibit lability in both sexes. In the duetting plain-tailed wren (Pheugopedius euophrys), males and females have auditory cells in the song system that are tuned to the joint song the two sexes produce rather than just male or female components. These findings suggest that there may be constraints on the adaptive response of the song system to ecological conditions as assessed by nucleus volume but that other critical variables regulating song can respond so that each sex can modify its song behaviour as needed.

Keywords: HVC; canary; sexual selection; song-control system.

Figure 1.

Schematic of the song-control system of songbirds illustrating the two main pathways connecting nucleus HVC (initially Hyperstriatum Ventrale pars caudale, now acronym used as proper name) to the nucleus robustus arcopallialis (RA). The caudal motor pathway (black arrows) directly connects HVC to RA and then to the motoneurons innervating the syrinx located in the tracheosyringeal part of the XIIth cranial nerve (nXIIts) and to two nuclei controlling respiration, the nucleus retroambigualis (RAm) and the rostral ventral respiratory group of neurons (rVRG). The anterior forebrain pathway (dotted arrows) also connects HVC to RA but via the area X of the striatum, the dorsolateral thalamic nucleus (DLM) and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). The medial preoptic nucleus is also represented; although it does not connect directly to the song system, testosterone action in this nucleus enhances the singing motivation. HVC, RA and X tend to exhibit male-biased sex differences in nucleus volume (see text for discussion).

Figure 2.

Photomicrographs illustrating the sex difference in RA in zebra finches (a,b) and European starlings (Sturnus vulgaris) (c,d). Male sections are in the left column (a and c) while females are in the right column (b,d). Note that the sex difference is more extreme in the case of the zebra finch where females do not sing (though they produce calls) than is for starlings where females are known to produce some song though not as frequently or as complex as male song [ and 17].

Figure 3.

Example responses in HVC to song stimuli in the duetting species the plain-tailed wren. Responses recorded in Ecuador in a female (a–d) and a male (e–h) wren. The bottom of each panel shows the stimulus oscillogram, at the top are raster plots showing the times of spikes for 20 stimulus repetitions, and in the middle is a histogram (50 ms bins) of the activity. Magenta indicates syllables produced by the female, blue by the male. Stimuli were (a,e) duet song, (b,f) female syllables, (c,g) male syllables and (d,h) reverse duet song. The female recording shown here had a strong preference for duet song over all other stimuli tested. The male recording shown here responded best to the duet song but, nonetheless, had a particularly strong response to the female syllables. Note that males and females respond best to the shared duet song (adapted from [48]).