Female Songbirds: The unsung drivers of courtship behavior and its neural substrates

Highlights

• Female songbirds play an important role in a broad range of social behavior.

• Female preferences are individual, malleable, and subject to social experience.

• Neural regions for song appear to modulate courtship in non-singing females.

Abstract

Songbirds hold a prominent role in the fields of neurobiology, evolution, and social behavior. Many of these fields have assumed that females lacked the ability to produce song and have therefore treated song as a male-specific behavior. Consequently, much of our understanding regarding the evolution and neural control of song behavior has been driven by these assumptions. Here we review literature from diverse fields to provide a broader perspective of the role of females in vocal communication and courtship. Recent evidence indicates that song evolved in both males and females and instances of female song are still common. The specialized neural circuit known as the “song system,” which is necessary for singing in males, is also present in females, including those that do not sing, implying broader functions that include evaluating male song and controlling courtship behavior. In addition to having flexible, individualized preferences, females actively shape their social network through their interactions with males, females, and juveniles. We suggest that by developing more accurate hypotheses concerning the role of females we may better understand the evolution and neural mechanisms of song production and courtship behavior.

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.