25 Years of sensory drive: the evidence and its watery bias

Abstract

It has been 25 years since the formalization of the Sensory Drive hypothesis was published in the American Naturalist (1992). Since then, there has been an explosion of research identifying its utility in contributing to our understanding of inter- and intra-specific variation in sensory systems and signaling properties. The main tenet of Sensory Drive is that environmental characteristics will influence the evolutionary trajectory of both sensory (detecting capabilities) and signaling (detectable features and behaviors) traits in predictable directions. We review the accumulating evidence in 154 studies addressing these questions and categorized their approach in terms of testing for environmental influence on sensory tuning, signal characteristics, or both. For the subset of studies that examined sensory tuning, there was greater support for Sensory Drive processes shaping visual than auditory tuning, and it was more prevalent in aquatic than terrestrial habitats. Terrestrial habitats and visual traits were the prevalent habitat and sensory modality in the 104 studies showing support for environmental influence on signaling properties. An additional 19 studies that found no supporting evidence for environmental influence on signaling traits were all based in terrestrial ecosystems and almost exclusively involved auditory signals. Only 29 studies examined the complete coevolutionary process between sensory and signaling traits and were dominated by fish visual communication. We discuss biophysical factors that may contribute to the visual and aquatic bias for Sensory Drive evidence, as well as biotic factors that may contribute to the lack of Sensory Drive processes in terrestrial acoustic signaling systems.

Keywords: animal communication; sensory drive; sensory ecology; sexual selection.

Figure 1.

The Sensory Drive Model (modified from Endler 1992b). Steps coded in green represent the sensory component of the Sensory Drive model as the environment places selective forces on the evolution of sensory system properties for food detection but that also influences female mate choice criteria. Steps of the model that incorporate sensory exploitation are indicated by asteriesk. Steps colored in blue represent the signalling component of the Sensory Drive model describing the evolution of signaling characteristics (ornament features, behavioral displays, and choice of microhabitat for display) that are predictable products of environmental constraints and/or responses to environmentally shaped female response biases. Note that the environment is featured in both components (sensory and signal tuning), hence that box is bi-colored. Except for those arrows with text, the arrows indicate evolutionary relationships. The combined effects of microhabitat choice and behaviour have immediate effects on the signalling environment. Neural crest cells affect colour patterns directly but are developmentally related to other cells in the neural system. This is a new component of Sensory Drive.

Figure 2.

Frequency waffle plots of studies supporting and not supporting the sensory drive model by aquatic (red) or terrestrial (orange) habitats, including studies that evaluated the sensory component of the sensory drive model, studies that evaluated the signaling components of the sensory drive model, and studies that evaluate the complete model (both major components). Note for color blind readers (either deutanomaly or protanomaly) the aquatic blocks will appear a dark green and the terrestrial a dark yellow).

Figure 3.

Frequency waffle plots of studies supporting and not supporting the sensory drive model by sensory modality [vision (red), auditory (orange)] including studies that evaluated the sensory component of the sensory drive model, studies that evaluated the signaling components of the sensory drive model, and studies that evaluate the complete model (both major components). Note for color blind readers (either deutanomaly or protanomaly) the vision blocks will appear a dark green and the auditory a dark yellow).

Figure 4.

Frequency waffle plots of studies supporting and not supporting the sensory drive model by taxonomic group [supporting (red) and non-supporting (orange)] including studies that evaluated the sensory component of the sensory drive model, studies that evaluated the signalling components of the sensory drive model, and studies that evaluate the complete model (both major components). Note for color blind readers (either deutanomaly or protanomaly) the supporting blocks will appear a dark green and the non-supporting a dark yellow).