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Pupil constriction has important functional consequences for animal vision, yet the evolutionary mechanisms underlying diverse pupil sizes and shapes are poorly understood. We aimed to quantify the diversity and evolution of pupil shapes among amphibians and to test for potential correlations to ecology based on functional hypotheses. Using photographs, we surveyed pupil shape across adults of 1294 amphibian species, 74 families and three orders, and additionally for larval stages for all families of frogs and salamanders with a biphasic ontogeny. For amphibians with a biphasic life history, pupil shape changed in many species that occupy distinct habitats before and after metamorphosis. In addition, non-elongated (circular or diamond) constricted pupils were associated with species inhabiting aquatic or underground environments, and elongated pupils (with vertical or horizontal long axes) were more common in species with larger absolute eye sizes. We propose that amphibians provide a valuable group within which to explore the anatomical, physiological, optical and ecological mechanisms underlying the evolution of pupil shape.

Made available in DSpace on 2022-04-29T08:39:58Z (GMT). No. of bitstreams: 0 Previous issue date: 2022-01-01 The spectral characteristics of vertebrate ocular lenses affect the image of the world that is projected onto the retina, and thus help shape diverse visual capabilities. Here, we tested whether amphibian lens transmission is driven by adaptation to diurnal activity (bright light) and/or scansorial habits (complex visual environments). Spectral transmission through the lenses of 79 species of frogs and six species of salamanders was measured, and data for 29 additional frog species compiled from published literature. Phylogenetic comparative methods were used to test ecological explanations of variation in lens transmission and to test for selection across traits. Lenses of diurnal (day-active) and scansorial (climbing) frogs transmitted significantly less shortwave light than those of non-diurnal or non-scansorial amphibians, and evolutionary modelling suggested that these differences have resulted from differential selection. The presence of shortwave-transparent lenses was common among the sampled amphibians, which implies that many are sensitive to shortwave light to some degree even in the absence of visual pigments maximally sensitive in the UV. This suggests that shortwave light, including UV, could play an important role in amphibian behaviour and ecology. Shortwave-absorbing lens pigments likely provide higher visual acuity to diurnally active frogs of multiple ecologies and to nocturnally active scansorial frogs. This new mechanistic understanding of amphibian visual systems suggests that shortwave-filtering lenses are adaptive not only in daylight conditions but also in those scotopic conditions where high acuity is advantageous. Read the free Plain Language Summary for this article on the Journal blog. Department of Life Sciences The Natural History Museum Department of Herpetology California Academy of Sciences Department of Vertebrate Zoology National Museum of Natural History Smithsonian Institution Department of Biology Amphibian and Reptile Diversity Research Center The University of Texas at Arlington Department of Biology York University Ecology Evolution and Development Group Department of Wetland Ecology Estación Biológica de Doñana (CSIC) Departamento de Biodiversidade and Centro de Aquicultura (CAUNESP) I.B. Universidade Estadual Paulista Department of Biology The Pennsylvania State University Department of Biological Sciences Institute for the Environment Florida International University Programa de Pós-graduação em Conservação da Fauna Universidade Federal de São Carlos Division of Optometry & Visual Science School of Health Sciences City University of London Departamento de Biodiversidade and Centro de Aquicultura (CAUNESP) I.B. Universidade Estadual Paulista

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.

Most vertebrates use a combination of rod and cone photoreceptors to enable vision in conditions ranging from starlight to direct sunlight. Nocturnal geckos, however, have simplex retinas that contain only rods in terms of morphology and physiology, but these rods are thought to be derived from cones through an evolutionary process known as photoreceptor transmutation. To investigate this, we generated eye transcriptomes and analyzed patterns of phototransduction gene evolution in geckos in comparison to other reptiles. We confirm that geckos have lost several major components of the rod phototransduction pathway, including rod opsin (RH1), which we identified as a pseudogene in multiple genomes. We also identified a partial rod transducin transcript, but found no evidence of the protein in retinal sections. However, we find that geckos express several complete rod phototransduction transcripts in the eye, which may contribute to the rod-like physiology of nocturnal gecko photoreceptors. Finally, we found surprising evidence that even though photoreceptor transmutation evolved independently in geckos and snakes, they have experienced parallel shifts in selective constraint on phototransduction genes. These results implicate adaptive change in the underlying molecular machinery of visual transduction, in addition to the convergent changes in cellular morphology, during photoreceptor transmutation.

Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genome structure that provide insight into the evolution of amniote genomes. Analyses of the garter snake and other squamate reptile genomes highlight shifts in repeat element abundance and expansion within snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z and W sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionary origins in a rear-fanged colubrid snake, together with new genomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

Convergent evolution in response to similar selective pressures is a well-known phenomenon in evolutionary biology. Less well understood is how selection drives convergence in protein function, and the underlying mechanisms by which this can be achieved. Here we investigate functional convergence in the visual system of two distantly related lineages of high-altitude adapted Andean and Himalayan catfishes. Statistical analyses revealed in the two high-altitude lineages, a parallel acceleration of evolutionary rates in rhodopsin, the dim-light visual pigment. However, the elevated rates were found to be accompanied by substitutions at different sites in the protein. Experiments substituting Andean- or Himalayan-specific residues significantly accelerated the kinetic rates of rhodopsin, destabilizing the ligand-bound forms. As found in cold-adapted enzymes, this phenotype likely compensates for a cold-induced decrease in kinetic rates, properties of rhodopsin mediating rod sensitivity and visual performance. Our study suggests that molecular convergence in protein function can be driven by parallel shifts in evolutionary rates but via non-parallel molecular mechanisms. Signatures of natural selection may therefore be a powerful guide for identifying complex instances of functional convergence across a wider range of protein systems. This article is protected by copyright. All rights reserved

The nocturnal origin of mammals is a longstanding hypothesis that is considered instrumental for the evolution of endothermy, a potential key innovation in this successful clade. This hypothesis is primarily based on indirect anatomical inference from fossils. Here, we reconstruct the evolutionary history of rhodopsin--the vertebrate visual pigment mediating the first step in phototransduction at low-light levels--via codon-based model tests for selection, combined with gene resurrection methods that allow for the study of ancient proteins. Rhodopsin coding sequences were reconstructed for three key nodes: Amniota, Mammalia, and Theria. When expressed in vitro, all sequences generated stable visual pigments with λMAX values similar to the well-studied bovine rhodopsin. Retinal release rates of mammalian and therian ancestral rhodopsins, measured via fluorescence spectroscopy, were significantly slower than those of the amniote ancestor, indicating altered molecular function possibly related to nocturnality. Positive selection along the therian branch suggests adaptive evolution in rhodopsin concurrent with therian ecological diversification events during the Mesozoic that allowed for an exploration of the environment at varying light levels.

Three complete mitochondrial genomes of South American electric fishes (Gymnotiformes), derived from high-throughput RNA sequencing (RNA-Seq), are reported herein. We report the complete mitochondrial genome of the bluntnose knifefish Brachyhypopomus n.sp. VERD, determined from newly sequenced data. We also provide the complete mitochondrial genomes for Sternopygus arenatus and the electric eel Electrophorus electricus, assembled from previously published transcriptome data. The mitochondrial genomes of Brachyhypopomus n.sp. VERD, Sternopygus arenatus and Electrophorus electricus have 13 protein-coding genes, 1 D-loop, 2 ribosomal RNAs and 22 transfer RNAs, and are 16,547, 16,667 and 16,906 bp in length, respectively. Phylogenetic analysis of the eight available mitochondrial genomes of gymnotiform fishes shows Apteronotus to be the sister lineage of other gymnotiformes, contradicting the “Sinusoidea” hypothesis that Apteronotidae and Sternopygidae are sister taxa.

Studies of cichlid evolution have highlighted the importance of visual pigment genes in the spectacular radiation of the African rift lake cichlids. Recent work, however, has also provided strong evidence for adaptive diversification of riverine cichlids in the Neotropics, which inhabit environments of markedly different spectral properties from the African rift lakes. These ecological and/or biogeographic differences may have imposed divergent selective pressures on the evolution of the cichlid visual system. To test these hypotheses, we investigated the molecular evolution of the dim-light visual pigment, rhodopsin. We sequenced rhodopsin from Neotropical and African riverine cichlids and combined these data with published sequences from African cichlids. We found significant evidence for positive selection using random sites codon models in all cichlid groups, with the highest levels in African lake cichlids. Tests using branch-site and clade models that partitioned the data along ecological (lake, river) and/or biogeographic (African, Neotropical) boundaries found significant evidence of divergent selective pressures among cichlid groups. However, statistical comparisons among these models suggest that ecological, rather than biogeographic, factors may be responsible for divergent selective pressures that have shaped the evolution of the visual system in cichlids. We found that branch-site models did not perform as well as clade models for our data set, in which there was evidence for positive selection in the background. One of our most intriguing results is that the amino acid sites found to be under positive selection in Neotropical and African lake cichlids were largely nonoverlapping, despite falling into the same three functional categories: spectral tuning, retinal uptake/release, and rhodopsin dimerization. Taken together, these results would imply divergent selection across cichlid clades, but targeting similar functions. This study highlights the importance of molecular investigations of ecologically important groups and the flexibility of clade models in explicitly testing ecological hypotheses.

Snakes possess many extreme morphological and physiological adaptations. Identification of the molecular basis of these traits can provide novel understanding for vertebrate biology and medicine. Here, we study snake biology using the genome sequence of the Burmese python (Python molurus bivittatus), a model of extreme physiological and metabolic adaptation. We compare the python and king cobra genomes along with genomic samples from other snakes and perform transcriptome analysis to gain insights into the extreme phenotypes of the python. We discovered rapid and massive transcriptional responses in multiple organ systems that occur on feeding and coordinate major changes in organ size and function. Intriguingly, the homologs of these genes in humans are associated with metabolism, development, and pathology. We also found that many snake metabolic genes have undergone positive selection, which together with the rapid evolution of mitochondrial proteins, provides evidence for extensive adaptive redesign of snake metabolic pathways. Additional evidence for molecular adaptation and gene family expansions and contractions is associated with major physiological and phenotypic adaptations in snakes; genes involved are related to cell cycle, development, lungs, eyes, heart, intestine, and skeletal structure, including GRB2-associated binding protein 1, SSH, WNT16, and bone morphogenetic protein 7. Finally, changes in repetitive DNA content, guanine-cytosine isochore structure, and nucleotide substitution rates indicate major shifts in the structure and evolution of snake genomes compared with other amniotes. Phenotypic and physiological novelty in snakes seems to be driven by system-wide coordination of protein adaptation, gene expression, and changes in the structure of the genome.

The pachycephalosaurian squamosal is one of the most diagnostic bones in this enigmatic group of dinosaurs, but little is known about variation in its morphology. Despite this, features of squamosal morphology are often used in diagnoses and phylogenetic studies. The recently proposed hypothesis of an ontogenetic transition from Dracorex to Pachycephalosaurus implies a large amount of ontogenetic variation in squamosal ornamentation that has not been well documented due to the small number of squamosals for these taxa. Stegoceras validum provides an important model for examining variation in squamosal morphology due to the large number of squamosals available. Here we examine the morphology of 14 S. validum squamosals both qualitatively and quantitatively. We find that although both node number and shape vary considerably, there is no clear ontogenetic pattern, which suggests a high degree of individual variation. The ornamental pattern, however, is maintained throughout the sample. Increase in n...

Colepiocephale lambei from the Foremost Formation of Alberta is a problematic pachycephalosaurid that has recently been hypothesized as (1) synonymous with Stegoceras validum, (2) a distinct species within the Stegoceras clade, and (3) an unusual taxon more derived than Stegoceras. Conflict among these hypotheses arises from different interpretations of the parietosquamosal region of the dome. Re-evaluation of the morphology of C. lambei based on all known material from Alberta indicates that the posteromedial extension of the parietal is broken off at its base in every specimen, and what was interpreted as the posterior margin of the dome actually is the anterior margins of large supratemporal fenestrae. The squamosals are not preserved in any specimen, but the form of the parietal suggests that they were present in the typical pachycephalosaurid configuration. Colepiocephale lambei is considered to be a distinct taxon based on several autapomorphies and stratigraphic segregation from S. validum...

The nocturnal origin of mammals is a longstanding hypothesis that is considered instrumental for the evolution of endothermy, a potential key innovation in this successful clade. This hypothesis is primarily based on indirect anatomical inference from fossils. Here, we reconstruct the evolutionary history of rhodopsin--the vertebrate visual pigment mediating the first step in phototransduction at low-light levels--via codon-based model tests for selection, combined with gene resurrection methods that allow for the study of ancient proteins. Rhodopsin coding sequences were reconstructed for three key nodes: Amniota, Mammalia, and Theria. When expressed in vitro, all sequences generated stable visual pigments with λMAX values similar to the well-studied bovine rhodopsin. Retinal release rates of mammalian and therian ancestral rhodopsins, measured via fluorescence spectroscopy, were significantly slower than those of the amniote ancestor, indicating altered molecular function possibly related to nocturnality. Positive selection along the therian branch suggests adaptive evolution in rhodopsin concurrent with therian ecological diversification events during the Mesozoic that allowed for an exploration of the environment at varying light levels.