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.

Polarization of light, and visual sensitivity to it, is pervasive across aquatic and terrestrial environments. Documentation of invertebrate use of polarized light is widespread from navigation and foraging to species recognition. However, studies demonstrating that polarization body patterning serves as a communication signal (e.g., with evidence of changes in receiver behavior) are rare among invertebrate taxa and conspicuously absent among vertebrates. Here, we investigate polarization-mediated communication by northern swordtails, Xiphophorus nigrensis, using a custom-built videopolarimeter to measure polarization signals and an experimental paradigm that manipulates polarization signals without modifying their brightness or color. We conducted mate choice trials in an experimental tank that illuminates a pair of males with light passed through a polarization filter and a diffusion filter. By alternating the order of these filters between males, we presented females with live males that differed in polarization reflectance by >200% but with intensity and color differences below detection thresholds (∼5%). Combining videopolarimetry and polarization-manipulated mate choice trials, we found sexually dimorphic polarized reflectance and polarization-dependent female mate choice behavior with no polarization-dependent courtship behavior by males. Male swordtails exhibit greater within-body and body-to-background polarization contrast than females, and females preferentially associate with high-polarization–reflecting males. We also found limited support that males increase polarization contrast in social conditions over asocial conditions. Polarization cues in mate choice contexts may provide aquatic vertebrates with enhanced detection of specific display features (e.g., movements, angular information), as well as a signaling mechanism that may enhance detection by intended viewers while minimizing detection by others.

Predator evasion in the open ocean is difficult because there are no objects to hide behind. The silvery surface of fish plays an important role in open water camouflage. Various models have been proposed to account for the broadband reflectance by the fish skin that involve one-dimensional variations in the arrangement of guanine crystal reflectors, yet the three-dimensional organization of these guanine platelets have not been well characterized. Here, we report the three-dimensional organization and the optical properties of integumentary guanine platelets in a silvery marine fish, the lookdown (Selene vomer). Our structural analysis and computational modelling show that stacks of guanine platelets with random yaw angles in the fish skin produce broadband reflectance via colour mixing. Optical axes of the guanine platelets and the collagen layer are aligned closely and provide bulk birefringence properties that influence the polarization reflectance by the skin. These data demonstrate how the lookdown preserves or alters polarization states at different incident polarization angles. These optical properties resulted from the organization of these guanine platelets and the collagen layer may have implications for open ocean camouflage in varying light fields.