The “Mute” Sex Revisited: Vocal Production and Perception Learning in Female Songbirds

Publisher Summary

Songbirds are known for their vocal versatility and the great developmental plasticity that permits or even makes it normal that adult signals are shaped by social learning processes. The chapter describes the vocal perception learning and vocal production learning in female songbirds. Song functions as an important mate attraction signal. Hence, it is often sexually dimorphic, with males typically the vocally displaying and advertising sex. The vocal perception learning in female song birds depends on recognition, song preferences, and perpetual fine tuning. Bird vocalizations are traditionally divided into calls and songs. The categorization is based both on physical characteristics of the signal (calls are shorter and less complex than songs) and also on its function. The chapter describes song learning and call learning in female song birds. Female song seems rare in comparison, and these behavioral dimorphisms also seem to map onto neuroanatomical differences in the specialized brain nuclei involved in singing. Consequently, there has been an emphasis on studying song acquisition in male songbirds. However, with female song described in a growing number of species, a new interest in the form and function of female song has surged. Likewise, theory has spawned interest in causes of variation on the receiver's side but also increasingly in the extent and function of female ornaments. With a culturally transmitted mating signal, learned preferences arise as an additional dimension next to genetically inherited and condition-dependent variation in female preferences and signaling.

Introduction

In almost all songbird species studied males sing, but differences in female song range from species where females have never been observed to sing to those where females sing as much as males. In male songbirds, song functions both as a territorial signal and a mate-attracting signal (Catchpole and Slater, 1995), and thus song is under sexual selection through male-male competition and female choice (Andersson, 1994). In the majority of species studied, males have been described as the vocally displaying, females the choosing sex. All the true songbirds (oscines), which comprise about half of the extant bird species, acquire at least part of their song by imitation (Catchpole and Slater, 1995). They are, by far, the best studied taxon among those documented to be vocal learners (Janik and Slater, 1997). However, a closer inspection of the literature shows that it has almost exclusively addressed the subject of vocal learning in male oscines. For example, the absence of the subject of female vocal learning is striking in all the most recent comprehensive reviews on bird song (Kroodsma 1982, Kroodsma 1996, Catchpole 1995).

While it is undisputed that many species show clear sex differences in song usage, vocal learning in female songbirds has been so little studied that a sex difference in vocal learning is less certain. Much of bird song research effort has been biased towards temperate zone species where female song is supposed to be rare compared to the tropics (Kroodsma et al., 1996) or to Australia (Robinson, 1949). However, this view has also changed recently. Female song in temperate zones might be rare in terms of absolute time spent singing, but in almost all of the more intensively studied species, females are reported to sing at least occasionally (reviews and references, e.g., Nice 1943, Ringleben 1982, Ritchison 1983a, Langmore 1998). Recent observational and experimental studies have revised the notion that “mute” females occasionally produce functionless song when in hormonal disbalance, and a number of hypotheses have been brought forward regarding the possible function of female song (reviews in Ritchison 1983a, Langmore 1998). This recent interest in female song has also revealed that its acquisition is poorly understood. For almost all species where both sexes sing it is unclear whether and how females learn their songs and whether they learn the same way as males do. A thorough understanding of the behavioral sex differences is paramount to studying the covarying neurophysiology and anatomy, but it is also necessary to understand the intricate interplay in gene-culture co-evolutionary processes.

With a culturally transmitted mating signal, the question arises of the extent to which cultural transmission in the actively advertising sex is paralleled in the choosing one. Song is an important factor in female choice, with different song attributes varying in their relative importance across species (Andersson 1994, Catchpole 1995, Searcy 1996). Given that songs are culturally transmitted, perception of oscine vocalizations, like their production, should show some developmental plasticity. Learning processes on the receiver's side might be essential to the dynamics of a communication system relying on culturally transmitted signals. Evidence is accumulating that female preferences for specific variants of conspecific acoustic signals are indeed greatly influenced by learning. The fact that song is often sexually dimorphic offers the unique opportunity to disentangle production from perception learning and to identify specialized adaptations of the brain. This is of great interest from a neuroethological point of view, especially to those focusing on mechanisms of learning and memory (Nottebohm 1990, MacDougall-Shackleton 1999, Bolhuis 2003). However, there has also been a recent surge of interest into perception learning from those with a more functionally and evolutionary orientated approach to behavior. While learning processes have now been acknowledged to contribute to variation between males, several authors have recently stressed that imprinting-like processes could play a far more important role in forming female preference than previously assumed (Owens 1999, ten Cate 1999). Developmental influences on female preferences are little understood, but have been identified as important sources for within-population variation in female preference (Jennions and Petrie, 1997). Therefore, an important first step is to map the distribution and extent of its occurrence.

It seems timely to review what is currently known on how learning processes influence female songbird perception, as well as the extent to which females learn their song and calls. This may provide a starting point for a more informed discussion on how earlier consideration of sex differences in vocal learning might have been at least partly confounded with sex differences in vocal performance. In addition, I hope to provide enough evidence for auditory perception learning in female songbirds to stimulate more research into receiver learning, as mating decisions exert selection pressures that are likely to have played an important role both in origin and maintenance of vocal learning.