Testosterone amplifies the negative valence of an agonistic gestural display by exploiting receiver perceptual bias

Abstract

Many animals communicate by performing elaborate displays that are incredibly extravagant and wildly bizarre. So, how do these displays evolve? One idea is that innate sensory biases arbitrarily favour the emergence of certain display traits over others, leading to the design of an unusual display. Here, we study how physiological factors associated with signal production influence this process, a topic that has received almost no attention. We focus on a tropical frog, whose males compete for access to females by performing an elaborate waving display. Our results show that sex hormones like testosterone regulate specific display gestures that exploit a highly conserved perceptual system, evolved originally to detect 'dangerous' stimuli in the environment. Accordingly, testosterone makes certain gestures likely to appear more perilous to rivals during combat. This suggests that hormone action can interact with effects of sensory bias to create an evolutionary optimum that guides how display exaggeration unfolds.

Keywords: aggression; perceptual bias; signal design; testosterone.

Figure 1.

(a) Bornean rock frog (Staurois parvus) foot-flagging. (b) Photos of different foot-flag components, with the blue circle and white line showing the foot's trajectory (white arrow = trajectory direction). Name of component is below each still (table 1). In coloured boxes above ii, iii and iv, we show how foot-flagging exploits feature analyser systems. Blue box (bottom) denotes different effective stimuli that underlie how conserved anuran feature analysers detect prey and environmental threats [–22]. Orange box (middle) describes the conserved behavioural responses elicited by effective stimuli [15], while green box (top) describes how these behavioural responses are exploited for socio-sexual communication through foot-flagging (proposed by [16,18]). (Online version in colour.)

Figure 2.

(a) Average shape of foot-flag from males given saline (control) or testosterone (T). White circle denotes foot origin and endpoint, with roman numerals corresponding to foot-flag phases (table 1). Red arrow shows the direction of foot movement. (b) Effects of T on shape characteristics encoded by principal component 1 (PC1), which represents the circularity of arch phases. (c–e) Effects of T on distance (mm) of foot-flag movements associated with feature analysers, including (c) extended-knee movements (worm-like), (d) arch movement (antiworm-like) and (e) pull-in movement (worm-like). Central lines on boxes denote mediate values, with the top and bottom denoting the 1st and 3rd quartiles, respectively. Whiskers denote 1.5 × the interquartile range, and asterisk denotes significance differences (p < 0.05). (Online version in colour.)

Figure 3.

LDA that assess whether effects of testosterone (T) on (a) foot-flag shape and (b) foot-flag speed are sufficient for discrimination between treatment groups. Horizontal axes show discriminate values, whereas vertical axes show frequencies of these values in each model. Orange bars (three bars on the right) = foot-flags from T males; blue bars (three bars on the left) = foot-flags from controls. Asterisks denote significant differences in the model, with corresponding kappa statistic (κ) to describe accuracy and non-randomness of the LDA categorization (see Methods). (Online version in colour.)