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

Abstract

The eyes of frogs and toads (Anura) are among their most fascinating features. Although several pupil shapes have been described, the diversity, evolution, and functional role of the pupil in anurans have received little attention. Studying photographs of more than 3200 species, we surveyed pupil diversity, described their morphological variation, tested correlation with adult habits and diel activity, and discuss major evolutionary patterns considering iris anatomy and visual ecology. Our results indicate that the pupil in anurans is a highly plastic structure, with seven main pupil shapes that evolved at least 116 times during the history of the group. We found no significant correlation between pupil shape, adult habits, and diel activity, with the exception of the circular pupil and aquatic habits. The vertical pupil arose at least in the most-recent common ancestor of Anura + Caudata, and this morphology is present in most early-diverging anuran clades. Subsequently, a horizontal pupil, a very uncommon shape in vertebrates, evolved in most neobatrachian frogs. This shape evolved into most other known pupil shapes, but it persisted in a large number of species with diverse life histories, habits, and diel activity patterns, demonstrating a remarkable functional and ecological versatility.

Diversity and evolution of amphibian pupil shapes

“…retinal streaks), but this hypothesis is not supported in the birds, mammals and fishes examined to date (Douglas, 2018). The variation in amphibian pupil shape we documented in the present study is consistent with a recently published, independent study of pupil shape in frogs and salamanders (Cervino et al, 2021), and warrants further attention with respect to the underlying musculature of the iris, latency and extent of the pupillary response, presence of multifocal lenses, and arrangement of photoreceptor cells in the retina to better understand the functional consequences of this diversity.…”

“…Because we relied on photographs to classify pupil shapes rather than on experimentally assessing pupillary response, our determination of 'oval' vs. 'slit' pupil shapes were limited by the available photos. However, our approach is similar to that of several recently published studies that quantified vertebrate pupil shape from photographs (Brischoux et al, 2010;Banks et al, 2015;Cervino et al, 2021) and provides a more taxonomically and developmentally extensive survey of pupil constriction diversity in amphibians than is currently feasible with experimental approaches.…”

“…1; Supporting Information, Figs S1, S2). We also compared our classifications to two recently published datasets that categorized pupil shape in adult frogs and salamanders (Yovanovich et al, 2020;Cervino et al, 2021;Supporting Information, Part C). phylogeny We used the phylogenetic hypothesis of Jetz & Pyron (2018) for visualizing trait distributions and modelling trait evolution across species.…”

“…By contrast, within mammals, squamates (lizards and snakes) and amphibians (frogs, salamanders and caecilians), constricted pupils include different non-elongated, vertically elongated and horizontally elongated shapes (Douglas, 2018), and there is some evidence that different pupil shapes correspond to differences in visual ecology among species. For instance, circular pupils are typical of teleost fishes (Douglas, 2018) and aquatic amphibians (Cervino et al, 2021), though the factors driving this are not well understood. Vertically elongated pupils in elapid snakes (cobras, mambas and marine snakes) are correlated with diel activity and foraging mode: the constricted pupils of nocturnal species that are ambush predators are vertical, whereas those of diurnal species that are active foragers are circular (Brischoux et al, 2010).…”

“…Although amphibian pupil shape has been studied in the context of species identification and systematics in some lineages (e.g. Drewes, 1984;Glaw & Vences, 1997;Nuin & do Val, 2005;Rödel et al, 2009;Menzies & Riyanto, 2015), and more recently with respect to evolutionary lability (Cervino et al, 2021), the functional consequences of different pupil shapes in amphibians are poorly understood. The limbless caecilian amphibians (order Gymnophiona, c. 200 extant species) are predominantly fossorial with greatly reduced visual systems, including eyes covered by skin and/or bone in many lineages (Walls, 1942;Wake, 1985;Wilkinson, 1997;Mohun et al, 2010).…”