Female Songbirds: The unsung drivers of courtship behavior and its neural substrates
Introduction
Songbirds (birds of the group Passeri) have been central to ecological and evolutionary thought for centuries and are one of the few groups of animals with learned vocalizations (alongside humans and a few others (Nowicki and Searcy, 2014, Nottebohm, 1972). The identification of a specialized neural circuit for song production (often called the “song system”) has made songbirds an important model for the study of vocal learning (Brainard and Doupe, 2013, Doupe and Kuhl, 1999) and motor control (Suthers and Margoliash, 2002). Throughout the history of songbird research, particularly amongst neurobiologists, much of the focus has been on active signalling by males. Females, in contrast, were viewed primarily as signal receivers and choosers. (Nottebohm and Arnold, 1976, Searcy and Andersson, 1986). This view has likely biased the study of courtship behavior and its neural bases to overlook the importance and complexity of female behavior (Jennions and Petrie, 1997), beyond its established role of driving evolution through mate-choice (Trivers, 1972). Increasing evidence suggests that female song is much more prevalent than once believed (Langmore, 2000, Riebel et al., 2005, Odom et al., 2014). This has far-reaching implications for how we understand the evolutionary origins of the avian communication system, even for species where female song has been lost (Price, 2015; Riebel, 2016). Here we review literature from various disciplines, focusing on the active role non-singing females play in mating interactions, the putative neural circuits that support and modulate these communicative behaviors, and the role that female behavior plays in driving social interaction.
Section snippets
The evolution of female choice
Females generally must invest more in their own offspring than males (Trivers, 1972) and therefore have strong incentives for selectivity in their mating choices. Assuming females can choose with whom they mate, these choices become a strong selective factor on males, driving male characteristics within the population in the direction of female preferences. This simple model was proposed by Darwin and more rigorously developed by Fisher as a mechanism to explain traits which otherwise appeared
Social malleability of female song preferences
Female preferences have typically been considered a means for females to select quality males based either on direct benefits (e.g. territory, parental care, nest defense) or indirect benefits (i.e. good genes (Andersson, 1994)). In comparison to male variation, little attention has been given to how song preferences may vary across or within individuals: if female song preferences evolved to obtain a single best mate, and if each female could obtain the same optimal male, preferences need not
A putative neural circuit for CSD production and mate choice
The neural mechanisms that underlie CSD production and its selectivity in female songbirds have not been studied in a rigorous fashion and as such the precise neural circuitry for this behavior remains poorly understood. Given the similarity of CSD behavior to the lordosis response in mammals, there is a strong likelihood that homologous circuits in the brainstem and spinal cord are engaged during CSD behavior. Furthermore, because CSD is a hormonally-dependent behavior that can be driven by
Discussion
Females have unique evolutionary pressures that encourage nuanced song preferences, which are individually variable and subject to a number of social factors. Mounting evidence points to the “song system” as a putative circuit for female courtship interactions where selectivity of female mating posture can be modulated by the same brain regions that drive song production in the male. While we have focused on CSD selectivity, these brain regions impact a range of behaviors in both male and
Conclusion
We have argued that across the fields of songbird research, we must modify our assumptions regarding the evolution and function of birdsong. While the ability to reduce a complex system to a tractable model is central to scientific investigation, and rewards from increased complexity of models diminish rapidly, it is abundantly clear that female songbirds have functional neural pathways and relevant social behaviors that impact a broad range of social interactions. A failure to acknowledge
Conflicts of interest
None.
Acknowledgements
We wish to thank the reviewers for their constructive comments. Authors also wish to acknowledge funding from the National Science Foundation: NSF IOS- 1557499, as well as Chloe Perkes and Karan Odom for their valuable feedback.
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