Ocular lens morphology is influenced by ecology and metamorphosis in frogs and toads

Abstract

The shape and relative size of an ocular lens affect the focal length of the eye, with consequences for visual acuity and sensitivity. Lenses are typically spherical in aquatic animals with camera-type eyes and axially flattened in terrestrial species to facilitate vision in optical media with different refractive indices. Frogs and toads (Amphibia: Anura) are ecologically diverse, with many species shifting from aquatic to terrestrial ecologies during metamorphosis. We quantified lens shape and relative size using 179 micro X-ray computed tomography scans of 126 biphasic anuran species and tested for correlations with life stage, environmental transitions, adult habits and adult activity patterns. Across broad phylogenetic diversity, tadpole lenses are more spherical than those of adults. Biphasic species with aquatic larvae and terrestrial adults typically undergo ontogenetic changes in lens shape, whereas species that remain aquatic as adults tend to retain more spherical lenses after metamorphosis. Further, adult lens shape is influenced by adult habit; notably, fossorial adults tend to retain spherical lenses following metamorphosis. Finally, lens size relative to eye size is smaller in aquatic and semiaquatic species than other adult ecologies. Our study demonstrates how ecology shapes visual systems, and the power of non-invasive imaging of museum specimens for studying sensory evolution.

Keywords: CT scanning; adaptation; eye; morphological evolution; sensory biology; visual ecology.

Figure 1.

MicroCT scan slice images of larvae (tadpole silhouette) and adults (frog silhouette) illustrating lens shape across metamorphosis for two anuran species with different adult habits. (a) The Schismaderma carens tadpole (aquatic) has spherical lenses that (b) flatten axially in the ground-dwelling (terrestrial) adult. (c) Spherical lenses of the Xenopus victorianus tadpole are (d) retained in the aquatic adult.

Figure 2.

Variation in ocular lens shape across anuran adults (121 species) and tadpoles (50 species). (a) Principal component analysis (PCA) of metrics used to quantify 3D lens shape (anisotropy, sphericity and elongation), with ellipses showing the 95% confidence level for a multivariate normal distribution in adults (black) and tadpoles (grey). Arrows indicate direction and weighting of vectors representing the three shape metrics analysed. Adults (filled circles) and tadpoles (unfilled circles) are partially separated along principal component (PC) 1. (b–d) Violin plots depict data for each shape metric across life stages. Tadpoles and adults differ significantly in lens (b) anisotropy and (c) sphericity, but not (d) elongation. Note that the y-axes differ on b–d; all three metrics are proportional values theoretically ranging from 0 to 1, but axes have been trimmed to match the range of data. The dashed line indicates the value of each shape metric for a perfect sphere, and the dotted line the value for a sphere flattened anteriorly in rough approximation of a typical terrestrial adult frog lens.

Figure 3.

Anuran lens shape across life stages, environments and adult habits. (a) Anuran phylogeny of 126 species across 41 families (adapted from [27]). Variation in lens shape is depicted with PC1 scores and the difference between PC1 scores of tadpoles (unfilled circles) and adults (filled circles, coloured by adult habit or black if habit unknown). (b) Anisotropy and (c) sphericity within species (n = 45) change significantly less in species with aquatic tadpoles that metamorphose into aquatic adults (blue) than for aquatic tadpoles that metamorphose into terrestrial adults (brown). Tadpole lens data are shown with unfilled circles and adult data with filled circles, with lines connecting data within each species. The dashed line indicates the value of each shape metric for a perfect sphere, and the dotted line the value for a sphere flattened anteriorly in rough approximation of a typical terrestrial adult frog lens.

Figure 4.

Adult anuran lens shape (n = 119) and relative size (n = 81) across species with different adult habits. (a) PCA centroids show multivariate adult lens shape across habits. Violin and box plots are ordered by mean and show lens (b) anisotropy, (c) sphericity and (d) relative size (residuals of a PGLS of lens diameter versus eye diameter) across adult habits. Letters above violin plots (a, b or c) indicate groups that are not significantly different from one another in multiple pairwise comparisons. The dashed line indicates the value of each shape metric for a perfect sphere, and the dotted line the value for a sphere flattened anteriorly in rough approximation of a typical terrestrial adult frog lens.