Eye‐body allometry across biphasic ontogeny in anuran amphibians

Abstract

Animals with biphasic lifecycles often inhabit different visual environments across ontogeny. Many frogs and toads (Amphibia: Anura) have free-living aquatic larvae (tadpoles) that metamorphose into adults that inhabit a range of aquatic and terrestrial environments. Ecological differences influence eye size across species, but these relationships have not yet been explored across life stages in an ontogenetic allometric context. We examined eye-body size scaling in a species with aquatic larvae and terrestrial adults, the common frog Rana temporaria, using a well-sampled developmental series. We found a shift in ontogenetic allometric trajectory near metamorphosis indicating prioritized growth in tadpole eyes. To explore the effects of different tadpole and adult ecologies on eye-body scaling, we expanded our taxonomic sampling to include developmental series of eleven additional anuran species. Intraspecific eye-body scaling was variable among species, with 8/12 species exhibiting a significant change in allometric slope between tadpoles and adults. Traits categorizing both tadpole ecology (microhabitat, eye position, mouth position) and adult ecology (habitat, activity pattern) across species had significant effects on allometric slopes among tadpoles, but only tadpole eye position had a significant effect among adults. Our study suggests that relative eye growth in the preliminary stages of biphasic anuran ontogenies is somewhat decoupled and may be shaped by both immediate ecological need (i.e. tadpole visual requirements) and what will be advantageous during later adult stages.

Diversity and evolution of amphibian pupil shapes

“…In particular, species that remain in aquatic habitats as adults retain non-elongated, round pupils whereas many species that occupy non-aquatic habitats as adults exhibit all three major axes of pupil constriction. Thus, our results are consistent with other studies of the visual system in larval and adult amphibians demonstrating that eye-body scaling (Shrimpton et al, 2021), lens . CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.…”

“…In particular, species that remain in aquatic habitats as adults retain non-elongated, round pupils whereas many species that occupy non-aquatic habitats as adults exhibit all three major axes of pupil constriction. Thus, our results are consistent with other studies of the visual system in larval and adult amphibians demonstrating that eye-body scaling (Shrimpton et al, 2021), lens shape (Sivak & Warburg, 1980;Sivak & Warburg, 1983), and whole-eye gene expression (Schott et al, in review) are decoupled when larvae and adults inhabit different light environments.…”

“…Once we had surveyed representatives of each family or sub-family, we expanded our sampling to encompass species that were the focus of recent studies on anuran visual biology (e.g., Thomas et al, 2020;Thomas et al, in review;Shrimpton et al, 2021) to maximize overlap with existing datasets. Preliminary assessments of this diversity suggested that pupil shape was diverse and/or evolutionarily labile in particular lineages and thus we elected to sample these groups in more depth.…”

“…During amphibian metamorphosis, dramatic morphological and physiological changes occur, including alterations to the visual system (Hoskins, 1990). Changes in eye-body scaling (Shrimpton et al, 2021) and lens shape (Sivak & Warburg, 1980;Sivak & Warburg, 1983) across ontogeny in frogs suggest that several structural aspects of the visual system adapt to both tadpole and adult visual requirements. Likewise, whole-eye differential expression of aquatic tadpoles versus terrestrial juvenile frogs (Schott et al, in review) demonstrates changes in a suite of visual genes related to eye and retinal development, light detection, lens crystallins, and phototransduction, indicating substantial decoupling between life stages at the level of gene expression.…”

A closer look at pupil diversity and evolution in frogs and toads

“…Pupil shape and its contractility are of major importance to deal with different light intensities and to establish a suitable compromise between high acuity and sensitivity [73,74]. However, pupil shape diversity is only one aspect of the eye that is relevant from the perspective of the evolution of visual perception, others being for example eye size [30,75], cornea and lens transmittance [27,28], lens optics [32,76], photoreceptor composition and size [25,26], oil droplets and visual pigments [77][78][79][80], and neural pathways [22,81].…”