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Lenses are vital components of well-functioning eyes and are crafted through the precise arrangement of proteins to achieve transparency and refractive ability. In addition to optical clarity for minimal scatter and absorption, proper placement of the lens within the eye is equally important for the formation of sharp, focused images on the retina. Maintaining these states is challenging due to dynamic and substantial post-embryonic eye and lens growth. Here, we gain insights into required processes through exploring the optical and visual consequences of silencing a key lens constituent inThermonectus marmoratussunburst diving beetle larvae. Using RNAi, we knocked down Lens3, a widely expressed cuticular lens protein during a period of substantial growth of their camera-type principal eyes. We show thatlens3RNAi results in the formation of opacities reminiscent of vertebrate lens ‘cataracts’, causing the projection of blurry and degraded images. Consequences of this are exacerbated in low-light conditions, evidenced by impaired hunting behaviour in this visually guided predator. Notably, lens focal lengths remained unchanged, suggesting that power and overall structure are preserved despite the absence of this major component. Further, we did not detect significant shifts in thein-vivorefractive states of cataract-afflicted larvae. This in stark contrast with findings in vertebrates, in which form-deprivation or the attenuation of image contrast, results in the dysregulation of eye growth, causing refractive errors such as myopia. Our results provide insights into arthropod lens construction and align with previous findings which point towards visual input being inconsequential for maintaining correctly focused eyes in this group. Our findings highlight the utility ofT. marmoratusas a tractable model system to probe the aetiology of lens cataracts and refractive errors. 

For eyes to maintain optimal focus, precise coordination is required between lens optics and retina position, a mechanism that in vertebrates is governed by genetics, visual feedback, and possibly intraocular pressure (IOP). While the underlying processes have been intensely studied in vertebrates, they remain elusive in arthropods, though visual feedback may be unimportant. How do arthropod eyes remain functional while undergoing substantial growth? Here, we test whether a common physiological process, osmoregulation, could regulate growth in the sophisticated camera-type eyes of the predatory larvae of Thermonectus marmoratus diving beetles. Upon molting, their eye-tubes elongate in less than an hour, and osmotic pressure measurements reveal that this growth is preceded by a transient increase in hemolymph osmotic pressure. Histological evaluation of support cells that determine the lens-to-retina spacing, reveals swelling rather than the addition of new cells. In addition, treating larvae with hyperosmotic media post-molt leads to far-sighted (hyperopic) eyes as expected from a failure of proper lengthening of the eye tube, and results in impaired hunting success. This study suggests that osmoregulation could be of ubiquitous importance for properly focused eyes. 

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.