How research on female vertebrates contributes to an expanded challenge hypothesis

Highlights

• This review applies the challenge hypothesis (CH) to females.

• Links between T and aggression are stronger in more persistent manipulations.

• Other steroidal and non-steroidal mechanisms may promote aggression when T is low.

• Novel data from the field shows how steroid sensitivity may influence T-behavior links.

• Extended CH must include molecular perspectives and tissue level effects of T.

Abstract

The bi-directional links between hormones and behavior have been a rich area of research for decades. Theory on the evolution of testosterone (T) was greatly advanced by the challenge hypothesis, which presented a framework for understanding interspecific, seasonal, and social variation in T levels in males, and how they are shaped by the competing demands of parental care and male-male competition. Female competition is also widespread in nature, although it is less clear whether or how the challenge hypothesis applies to females. Here, we evaluate this issue in four parts: (1) We summarize and update prior analyses of seasonal plasticity and interspecific variation in T in females. (2) We evaluate experimental links between T and female aggression on shorter timescales, asking how T manipulations affect aggression and conversely, how social manipulations affect T levels in female mammals, birds, lizards, and fishes. (3) We examine alternative mechanisms that may link aggression to the social environment independently of T levels in circulation. (4) We present a case study, including new data analyses, in an aggressive female bird (the tree swallow, Tachycineta bicolor) to explore how variation in tissue-level processing of T may bridge the gap between circulating T and variation in behavior that is visible to natural selection. We close by connecting these multivariate levels of sex steroid signaling systems alongside different temporal scales (social, seasonal, and evolutionary) to generate broadly applicable insights into how animals respond to their social environment, regardless of whether they are male or female.

Introduction

“Females are generally regarded as not aggressive and testosterone is regarded as the ‘male sex hormone.’ These views are incorrect…”

–Wingfield et al. (2000)

The sex steroid hormone testosterone (T) is thought to regulate phenotypic responses to dynamic social environments in male vertebrates. For instance, males typically produce more T during breeding stages that involve mating competition and less T during parental breeding stages (Ketterson and Nolan, 1992; Wingfield, 1984). Likewise, males may temporarily elevate T levels in response to a prospective rival or mate (Gleason et al., 2009; Wingfield, 1985). As a result, T levels may exceed what is necessary for reproduction, instead promoting behaviors that are adaptive during competition (Wingfield et al., 1990). Similar patterns may apply over evolutionary time, with higher T in species with heightened competition for territories or mates (Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2003; Oliveira et al., 2002). Patterns of T secretion across three timescales – social, seasonal, and evolutionary – form the crux of the challenge hypothesis, which broadly suggests that variation in T secretion within and among species stems from natural selection related to trade-offs between mating effort and parental effort (Wingfield, 2012; Wingfield et al., 1990, Wingfield et al., 2001).

This framework has been largely supported in males across many taxa (Archer, 2006; Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2003; Oliveira et al., 2002). However, we still have a relatively limited understanding of whether and how the challenge hypothesis applies to females. Our primary goal is to synthesize current data on the challenge hypothesis in females. In addition, we evaluate hypotheses that broaden the challenge hypothesis beyond its initial focus on T, asking how other hormones and tissue-level processes may modulate phenotypic responses to social competition. We begin by overviewing relationships between T and female behavior, including prior analyses of seasonal and interspecific variation in T. We then provide a novel synthesis of 80 previously published studies across vertebrate taxa to evaluate two key aspects of the challenge hypothesis: (H1) Elevated T promotes female aggression, and (H2) females respond to competition by elevating T. Next, we broaden our focus and begin to evaluate two related hypotheses: (H3) Other components of sex steroid signaling systems and (H4) non-steroidal mechanisms may influence aggression, independently of T levels in circulation, promoting the adaptive expression of aggression without necessitating elevated T per se. Finally, we describe a case study in an avian species with strong female-female competition to explore how tissue-level variation in sex steroid signaling systems may interact with seasonal patterning of T and aggression. We close by connecting these different mechanistic levels and temporal scales (social, seasonal, and evolutionary) to generate broad insights on the challenge hypothesis that are applicable not only to females but to both sexes.