A perspective on sensory drive

In 1992, The American Naturalist published a special supplement entitled: “Sensory Drive. Does Sensory Drive Biology Bias or Constrain the Direction of Evolution? ” organized by John Endler. The supplement contained a seminal paper on “sensory drive” by Endler (1992a) as well as several other well-cited papers on sensory exploitation (Ryan and Keddy-Hector 1992), background matching with respect to motion (Fleishman 1992), chemical cues in mammals and amphibians (Alberts 1992; Roth et al. 1992), and the relationship between auditory processing and call properties in frogs (Narins 1992). The paper by Endler was especially important; it has been cited over 1,200 times and has inspired research at many levels of ecology and evolution across diverse taxa and sensory modalities. In this paper and associated ones, Endler laid out the primary components that influence the evolution of signaling systems, placing a large emphasis on the environmental conditions under which signaling occurs (Endler 1992a, 1992b, 1993). Twenty-five years later, the American Society of Naturalists held a symposium on “25 Years of Sensory Drive” at the 2017 Evolution meetings in Portland, Oregon, organized by Becky Fuller. This special column in Current Zoology summarizes the work presented there as well as other contributions made for the column. In this editorial, we first review sensory drive and the state of the field when it emerged. We then summarize the work in this special column and suggest fruitful ways forward. Figure 1 shows the sensory drive framework. In order for signaling to occur between a signaler and a receiver the following must happen: The signaler gives off signal(s) using one or more signal modalities, and those signals have particular properties (e.g., reflectance, pitch, degree of polarization, chemical structure, etc.). The signals are given off in particular times and places. In order for the signal to be successful, the signal must travel through the environmental conditions under which signaling takes place and be detected by the receiver against a background of other potential stimuli. The signal is then detected (or not) by the sensory system of the receiver and processed by the brain, which influences the perception of the signals and the resulting behavior (i.e., decision criteria). Of course, there are other things can influence the evolution of the signaler and the receiver, which are indicated in Figure 1. The receiver must do many things with its sensory systems other than merely detect signals used in communication. It must also find food, avoid predators, and find proper habitat, all of which can exert natural selection on sensory system properties. In Figure 1, this is exemplified by “Detectability of food” and foraging success (fs). In addition, the act of signaling may make signalers more conspicuous to predators and other actors that would exploit signals. The environmental conditions under which signaling takes place can affect the roles of predators and eavesdroppers just as it can with signalers and intended receivers. Open in a separate window Figure 1 Diagram of the main processes in sensory drive, modified and revised from Endler (1992). Solid arrows indicate evolutionary processes. Dashed arrows with upper case symbols indicate immediate or functional effects: Eo: immediate effects of ecological and optical conditions on signalling conditions. V: immediate effect of microenvironment on the visibility of prey. P: immediate effect of microenvironment on visibility to predators, and also natural selection caused by microenvironmental conditions acting on predator senses and behaviour. Lower Case Symbols: Fs: feeding success that directly affects the evolution of the senses. Ms: mating success that affects sensory evolution directly. Ss: sexual selection (Good Genes, Fisher Process, etc.) That influences mate-choice criteria evolution directly. The asterisks identify the three components of sensory exploitation, a well-studied subset of sensory drive.