Selection on Visual Opsin Genes in Diurnal Neotropical Frogs and Loss of the SWS2 Opsin in Poison Frogs

Abstract

Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here, we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in frogs and some salamanders, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their behavior. Our analyses show that assessments of opsin diversification in across taxa could expand our understanding of the role of sensory system evolution in ecological adaptation.

Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments

“…There is strong evidence for the loss of SWS2 in dendrobatids, and corresponding loss of the blue-sensitive rods where SWS2 is typically expressed in frogs. We did not find SWS2 expressed in the dendrobatid eye transcriptomes, and another study was also unable to recover SWS2 from dendrobatid bait-capture data or an eye transcriptome ( Wan et al 2023 ); however, in the two dendrobatid genomes, we found short fragments that are likely pseudogene remnants of SWS2 , based on phylogenetic analysis. Furthermore, retinal microspectrophotometry (MSP) to estimate photoreceptor absorbance spectra did not detect blue-sensitive rods in the three dendrobatids examined here or the species examined previously ( Siddiqi et al 2004 ).…”

Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses

“…From left to right: an ultrametric tree showing phylogenetic relationships inferred previously [55] among sampled species with the three defended poison frog clades highlighted in purple, the undefended clades in dark gray, and non-dendrobatids in light gray (Bufonidae: Amazophrynella siona and Atelopus aff. spurrelli ; Leptodactylidae: Lithodytes lineatus ).…”

“…Therefore, data are not directly comparable, and they could not be included in Figure 3. Phylogenies were subsetted from [59] using ape v5.7.1 [94] and phytools v1.9.16 [95]. Any compounds known to co-elute with other compounds were unable to be identified, so we averaged their quantities across the co-eluting compounds.…”

Insights into the evolution of photoreceptor oil droplets in frogs and toads

“…Given that amphibians display a wide spectrum of ecological traits (habitat, rhythmic activity, reproductive mode, behaviour and colour patterns [26][27][28]), they represent an interesting group for understanding how properties of the visual system differ among diverse photic environments. In addition, recent studies began to explore different aspects of visual ecology in relation to both morphological and spectral variations, particularly in anuran eyes [29][30][31][32][33][34][35][36][37]. Still, knowledge of the taxonomic distribution of the ODs in anurans remains sparse owing to the patchiness of the studied species across the anuran phylogenetic diversity, hindering any evaluation of its evolution and relationship with visual ecology in the group [9].…”