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.

Sensory collectives in natural systems

“…Recent decades have witnessed huge advances in our understanding of the selective pressures shaping sensory system evolution in a large range of organs and organisms ( Melin et al, 2022 ; Moore et al, 2017 ; Oteiza and Baldwin, 2021 ; Zhao et al, 2009 ). Many research programs have focused on ecologically relevant stimuli and environments such as the impacts of light levels during activity on visual system evolution, including eye shape, size, and photoreceptor composition ( Mitra et al, 2022 ; Moritz et al, 2014 ; Peichl et al, 2000 ; Veilleux and Kirk, 2014 ), the organic compounds in potential foods and the types, structure, and distributions of taste receptors ( Baldwin et al, 2014 ; Chu et al, 2014 ; Cramer et al, 2022 ; Jiang et al, 2012 ; Toda et al, 2021 ; Zhao et al, 2015 ), and prey movements and the localisation and sensitivity of mechanical and electric receptors in predators ( Gardiner and Atema, 2007 ; Niesterok et al, 2017 ; Pohlmann et al, 2004 ; Schulte-Pelkum et al, 2007 ). Research into social factors and their impact on sensory evolution has also generated important insights.…”

Visual environment of rearing sites affects larval response to perceived risk

“…It is well established that the challenge in turbid waters is not light availability (and thus it cannot be straightforwardly overcome with increased sensitivity) but rather distance-dependent contrast degradation due to non-image forming scattered light (Lythgoe 1979). In this scenario, myopic eyes such as those of tadpoles might not be so disadvantageous after all (Mitra et al 2022), as the image quality of the visual scene is proportionately better when viewing objects close by. There are neither theoretical nor empirical estimates of tadpoles' visual acuity, however the recent confirmation that they tend to have spherical lenses even in species in which the adult lenses are flattened (Mitra et al 2022) opens up the possibility for tadpoles to present adaptations to maximise (within the constraints imposed by eye size) their spatial resolution and thus have a better chance to deal with turbid visual environments.…”

Convergent Anuran Middle Ear Loss Lacks a Universal, Adaptive Explanation

“…Thus, ear loss may only be puzzling when viewed through a lens that is focused on anuran acoustic communication. As research into other, less studied anuran sensory systems (e.g., vision - [58][59][60][61]; olfaction - [62,63]; vibration - [64][65][66]) and communication styles [67] increases, tympanic middle ear loss might not seem so odd from a frog's sensory standpoint.…”