Evolutionary ecology of chemosensation and its role in sensory drive

Abstract

All behaviors of an organism are rooted in sensory processing of signals from its environment, and natural selection shapes sensory adaptations to ensure successful detection of cues that maximize fitness. Sensory drive, or divergent selection for efficient signal transmission among heterogeneous environments, has been a useful hypothesis for describing sensory adaptations, but its current scope has primarily focused on visual and acoustic sensory modalities. Chemosensation, the most widespread sensory modality in animals that includes the senses of smell and taste, is characterized by rapid evolution and has been linked to sensory adaptations to new environments in numerous lineages. Yet, olfaction and gustation have been largely underappreciated in light of the sensory drive hypothesis. Here, we examine why chemosensory systems have been overlooked and discuss the potential of chemosensation to shed new insight on the sensory drive hypothesis and vice versa. We provide suggestions for developing a framework to better incorporate studies of chemosensory adaptation that have the potential to shape a more complete, coherent, and holistic interpretation of the sensory drive.

Keywords: chemical signaling; chemoreceptor; chemosensation; olfaction; sensory drive.

Figure 1.

The three components of sensory drive through the perspective of olfaction and how they may relate to one another in a mammalian community. Chemical signals must be transmitted through a complex chemical background composed of a general background of volatile organic compounds (VOCs) and intra- and interspecific chemical signals, all interacting with abiotic conditions such as wind and humidity. The perceiver expresses hundreds of different genes in a number of different chemosensory receptor gene families under selection to maximize individual fitness. Sensory drive research in chemosensory systems is required to understand how changing environments influence the evolution of chemical communication. Abbreviations of mammalian chemosensory receptors: ORs: olfactory receptors; TAARs: Trace amine-associated receptors; V1Rs: vomeronasal type-1 receptors; V2Rs: vomeronasal type-2 receptors; FPRs: formyl peptide receptors.

Figure 2.

The Iberian wall lizard Podarcis hispanicus illustrates a strong candidate for sensory drive promoting chemosensory divergence and local adaptation. Compounds of the male femoral gland excretions differ based on the environment, in which northern populations have waxier and bulkier compounds that are less volatile and enable more viable signals in the given habitat. Receptors of the perceivers are unknown, but behavioral evidence has demonstrated female preference and male–male recognition of signals based on their own environments. Silhouettes are from vecteezy and all-free-download.com.