Genomic and Spectral Visual Adaptation in Southern Leopard Frogs during the Ontogenetic Transition from Aquatic to Terrestrial Light Environments

Abstract

Many animals have complex life cycles where larval and adult forms have distinct ecologies and habitats that impose different demands on their sensory systems. While the adaptive decoupling hypothesis predicts reduced genetic correlations between life stages, how sensory systems adapt across life stages at the molecular level is not well understood. Frogs are a compelling system to study this question in because most species rely on vision as both aquatic tadpoles and terrestrial adults, but these habitats present vastly different light environments. Here we used whole eye transcriptome sequencing to investigate differential expression between aquatic tadpoles and terrestrial juveniles of the southern leopard frog (Lithobates sphenocephalus). Because visual physiology changes with light levels, we also tested how constant light or dark exposure affected gene expression. We found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles, versus 5% for light/dark exposure. Analyses targeting a curated set of visual genes revealed significant differential expression between life stages in genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Light/dark exposure had a significant effect on a smaller set of visual genes. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments. Overall, we identified extensive expression-level differences in the eyes of tadpole and juvenile frogs related to observed morphological and physiological changes through metamorphosis, and corresponding adaptive shifts to optimize vision in aquatic versus terrestrial environments.

Ecology drives patterns of spectral transmission in the ocular lenses of frogs and salamanders

“…Many amphibians have distinct life stages, and anurans are known to exhibit changes in visual systems at metamorphosis (e.g. Schott et al., 2021; Sivak et al., 1985; Shrimpton et al, 2021). Although we found that the tadpoles of two frog species had shortwave‐transparent lenses, the adult stage of Alytes muletensis also had shortwave‐transparent lenses (Figure 1b).…”

Tadpole Responses to Environments With Limited Visibility: What We (Don’t) Know and Perspectives for a Sharper Future

“…However, because these data come from adult individuals, it remains to be investigated if these filtering properties are already present in the tadpoles of relevant species, and whether larval stage could provide a compelling biological explanation for those cases in which the adult filtering pattern does not follow any immediately obvious logic. Interestingly, other recent work has found differences in expression levels of genes related to lens composition in tadpoles versus juveniles of the frog Lithobates sphenocephalus (Schott et al, 2021). If these gene products were ones to affect light transmittance in a wavelength-dependent manner (e.g., Röll, 2001), the finding would argue against the speculation outlined just above, and highlight the need to explore the issue in more species to find -or rule-out potential patterns.…”

“…While "immature" in the grand scheme of ontogeny, larvae are adapted to their aquatic habitats with the same degree of refinement with which adults are adapted to their environments post-metamorphosis (McDiarmid and Altig, 1999). Such a clearly defined biphasic life cycle, unparalleled among vertebrates, presents a unique opportunity to study the plasticity of visual systems: even within species the visual system can be differentially tuned to match the surrounding environment before and after metamorphosis, as has been shown for relative eye size (Shrimpton et al, 2021) and expression levels of genes that determine spectral sensitivity (Schott et al, 2021).…”

Evolutionary analyses of visual opsin genes in anurans reveals diversity and positive selection suggestive of functional adaptation to distinct light environments

“…Another possibility is that, in some anuran species, SWS1 is only expressed at certain life stages, such as in tadpoles. Ontogenetic shifts in expression of visual opsins is fairly common in teleost fishes (Carleton et al 2020), but the only study of expression profiles in a frog (L. sphenocephalus) found that SWS1 was expressed at a low, but consistent level in both tadpoles and postmetamorphic juvenile frogs (Schott et al 2021a).…”

“…Relative to other vertebrates, little is known about the diversity of photoreceptors and visual opsins in anurans and other amphibians. Four of the five visual opsin genes have been identified in anurans (RH1, LWS, SWS1, SWS2), but RH2 has not been found in any amphibian and is presumed to have been lost early during their evolution (Bowmaker 2008;Schott et al 2021a). These opsins may be found in as many as eight different photoreceptor types including two types of rods, one of which is unique to amphibians.…”