Evolution of Sensory Receptors

Abstract

Sensory receptors are at the interface between an organism and its environment and thus represent key sites for biological innovation. Here, we survey major sensory receptor families to uncover emerging evolutionary patterns. Receptors for touch, temperature, and light constitute part of the ancestral sensory toolkit of animals, often predating the evolution of multicellularity and the nervous system. In contrast, chemoreceptors exhibit a dynamic history of lineage-specific expansions and contractions correlated with the disparate complexity of chemical environments. A recurring theme includes independent transitions from neurotransmitter receptors to sensory receptors of diverse stimuli from the outside world. We then provide an overview of the evolutionary mechanisms underlying sensory receptor diversification and highlight examples where signatures of natural selection are used to identify novel sensory adaptations. Finally, we discuss sensory receptors as evolutionary hotspots driving reproductive isolation and speciation, thereby contributing to the stunning diversity of animals.

Keywords: chemoreceptors; ion channels; light receptors; mechanoreceptors; sensory drive; thermoreceptors.

Figure 1

Evolution of major sensory receptor families. Sensory gene repertoires show lineage-specific expansions and losses, with chemoreceptors exhibiting the most dynamic patterns of evolution. The phylogeny of major metazoan clades, as well as the closest relatives of animals, the choanoflagellates and filastereans, is shown. Lines at the nodes indicate inferred gains, and dotted lines denote inferred losses of receptor families. Colors in the heat map represent the normalized number of genes across columns. The heat map values correspond to the number of retrieved receptors for each family and species. Sensory receptor families are classified as mechanoreceptors, thermoreceptors, chemoreceptors, and light receptors: Piezo; transient receptor potential (TRP) channels, including TRPM (melastatin), TRPV (vanilloid), TRPA (ankyrin), TRPP (polycystin or polycystic kidney disease), and TRPN (including nompC, or no mechanorecaptor potential C); gustatory receptor (GR); odorant receptor, mainly present in vertebrates (OR-V); ionotropic receptor (IR); chemotactile receptor (CR); odorant binding protein (OBP) and insect odorant receptor (OR-I); nematode chemosensory (NEMCH) receptor; trace amine-associated receptor (TAAR); vomeronasal receptor type 1 (V1R); vomeronasal receptor type 2 (V2R); taste receptor type 1 (T1R); taste receptor type 2 (T2R); ciliary opsins (C-opsins); rhabdomeric opsins (R-opsins); retinal G protein–coupled receptor (RGR-Go) opsins; and other (cnidopsins, placopsins, and echinopsins). Here, we used OR-I to distinguish insect ORs from the unrelated vertebrate odorant receptors, here called OR-V. Figure animal silhouettes adapted from images from https://www.phylopic.org/.

Figure 2

Genomic architecture, protein structure, and membrane topology of sensory receptors, showing patterns of assembly. Exon-intron structures (green) of sensory receptor families hint at the duplication mechanism underlying their evolution. The exon-intron architectures and assemblies were inferred from the majority of the known cases within the gene families. Distinct families across vertebrates and invertebrates diverged from ancestral neurotransmitter receptors, including IRs, CRs, and TAARs. Piezo channels, TRP channels, GRs, ORs-I, IRs, and CRs are nonselective cation channels. GPCRs transduce information through multicomponent second messenger–based signaling pathways. Abbreviations: CRs, chemotactile receptors; GPCRs, G protein–coupled receptors; GRs, gustatory receptors; IRs, ionotropic receptors; ORs-I, insect olfactory receptors; OR-V, vertebrate odorant receptor; T1R, taste receptor type 1; T2R, taste receptor type 2; TAARs, trace amine-associated receptors; TRP, transient receptor potential; V1R, vomeronasal receptor type 1; V2R, vomeronasal receptor type 2.

Figure 3

Evolutionary mechanisms at the population level drive gene diversification. (a) There are four main evolutionary forces. Mutation introduces new variants into the population. Gene flow introduces new variants through migration from divergent populations. Genetic drift explains the increase or decrease of variant frequency in a population due to random processes and is linked to population size. Natural selection increases the frequency of genetic variants that increase population fitness, including survival and reproduction. (b) Duplications are the most common type of mutation underlying the evolution of novel gene families. Tandem duplications produce identical adjacent sequences. Retroduplications result in a retrocopy of the gene devoid of introns and with a polyA tail. Whole-genome duplication entails complete chromosome duplication. (c) Different types of natural selection decrease, shift, or increase genetic variation in a population. Stabilizing selection decreases genetic variation, favoring an average phenotype. Directional selection favors a particular phenotype, causing the frequency of variants to continuously shift in one direction. Diversifying selection (or disruptive selection) increases genetic variation as it favors two or more phenotypes, each providing selective advantages.

Figure 4

Detecting signatures of natural selection in the evolution of sensory receptors. (a) Selective sweep for the rapidly increased frequency of a black water–adapted blue-light-sensitive opsin (SWS2) variant in sticklebacks, which colonized dark water habitats after glaciation around 12,000 years ago. The black water–adapted sticklebacks were transplanted to a clear water habitat, and after 19 years, the alternate SWS2 clear water–adapted variant increased, consistent with a transient reversed selective sweep. (b) Archaic admixture into eastern gorillas includes adaptive introgression (adaptive transfer of variation between species through gene flow) of a taste receptor TAS2R14 variant. Since gorillas from eastern populations have more herbaceous diets than the frugivorous western gorillas, this introgression event likely shaped the adaptive perception of bitter taste in eastern gorillas. (c) TRPA1 channels underlie infrared perception in pit-bearing snakes. TRPA1 channels of pit-bearing snakes show accelerated rates of adaptive evolution compared to TRPA1 sequences of non-pit-bearing snakes. (d) Cephalopod CRs evolved from ancestral acetylcholine receptors. Key amino acid sites in the ligand-binding pocket of octopus CRs are under strong diversifying selection mediating the detection of hydrophobic molecules for contact-dependent aquatic chemosensation, in contrast to the ancestral detection of small polar neurotransmitters. Abbreviations: CRs, chemotactile receptors; LRT, likelihood ratio test. Panel a adapted from Marques et al. (2017) (CC BY 4.0). Panel b adapted from Pawar et al. (2023) (CC BY 4.0). Panel c adapted from Geng et al. (2011) (CC BY 4.0). Panel d adapted from Allard et al. (2023c). Illustrations of animals adapted from images created with BioRender.com.

Figure 5

Divergence in sensory receptors drives the evolution of new species and fuels adaptive radiations. (a) In moths, the composition of pheromone components is highly species-specific and promotes reproductive isolation between the sister species Heliothis virescens and Heliothis subflexa. A single critical amino acid mutation in OR6 changes receptor specificity to alter the preference of male moths for female sex pheromones of their own species. (b) Divergent evolution in the visual system of Lake Victoria cichlids is adapted to different depths and associated with male coloration and female preference for coloration of conspecific males, indicating reproductive isolation leading to speciation through sensory drive. (i) The sympatric pair of closely related cichlid species includes a red-colored species that exhibits a long-wavelength-sensitive (LWS) opsin haplotype adapted to the redshifted ambient light of the greater water depths it inhabits and a blue-colored species with a non-redshifted LWS opsin haplotype that is adapted to shallow, clear waters. (ii) Interspecific gene flow (hybridization) between these divergent lineages facilitated cichlid radiation by providing variation at the LWS locus, which is critically involved in adaptation and speciation. This case of gene flow underpinning the diversity of opsin haplotypes illustrates how evolutionary processes such as the gene flow of sensory receptor variants can facilitate adaptive radiations. Panel a adapted from Cao et al. (2021) (CC BY 4.0). Panel b, subpanel i adapted with permission from Seehausen et al. (2008). Panel b, subpanel ii adapted from Meier et al. (2017) (CC BY 4.0). Illustrations of animals adapted from images created with BioRender.com.