Morphology and evolution of the snake cornea

Da Silva M.O., Heegaard S., Wang T., Gade J.T., Damsgaard C., Bertelsen M.F.

Covering the eye of all snakes is a transparent integumental structure known as the spectacle. In order to determine variations in spectacle thickness among species, the spectacles of 217 alcohol-preserved museum specimens of 44 species belonging to 14 different families underwent optical coherence tomography (OCT) to measure spectacular thickness. Multivariable analyses were made to determine whether family, activity period (diurnal/nocturnal) and habitat (arboreal/terrestrial/fossorial/aquatic) influenced spectacle thickness. The thinnest spectacles in absolute terms were found in the Usambara bush viper (Viperidae) with a thickness of 74 ± 9 μm and the absolute thickest spectacle was found in the red-tailed pipe snake (Cylindrophiidae) which had a spectacle thickness of 244 ± 57 μm. Fossorial and aquatic snakes had significantly thicker spectacles than arboreal and terrestrial snakes. When spectacle thickness was correlated to eye size (horizontal spectacle diameter), Gray’s earth snake (Uropeltidae) had the lowest ratio (1:7) and the cottonmouth (Viperidae) had the highest ratio (1:65). Multivariable and phylogenetic analyses showed that spectacular thickness could be predicted by taxonomic family and habitat, but not activity period. This phylogenetically broad systematic study of the thickness of the snake spectacle showed that spectacular thickness varies greatly across snake species and may reflect evolutionary adaptation and development.

Zheng Y., Wiens J.J.

Two common approaches for estimating phylogenies in species-rich groups are to: (i) sample many loci for few species (e.g. phylogenomic approach), or (ii) sample many species for fewer loci (e.g. supermatrix approach). In theory, these approaches can be combined to simultaneously resolve both higher-level relationships (with many genes) and species-level relationships (with many taxa). However, fundamental questions remain unanswered about this combined approach. First, will higher-level relationships more closely resemble those estimated from many genes or those from many taxa? Second, will branch support increase for higher-level relationships (relative to the estimate from many taxa)? Here, we address these questions in squamate reptiles. We combined two recently published datasets, one based on 44 genes for 161 species, and one based on 12 genes for 4161 species. The likelihood-based tree from the combined matrix (52 genes, 4162 species) shared more higher-level clades with the 44-gene tree (90% vs. 77% shared). Branch support for higher level-relationships was marginally higher than in the 12-gene tree, but lower than in the 44-gene tree. Relationships were apparently not obscured by the abundant missing data (92% overall). We provide a time-calibrated phylogeny based on extensive sampling of genes and taxa as a resource for comparative studies.

Lauridsen H., Da Silva M.O., Hansen K., Jensen H.M., Warming M., Wang T., Pedersen M.

Nineteen clinically normal snakes: six ball pythons (Python regius), six Burmese pythons (Python bivittatus), one Children’s python (Antaresia childreni), four Amazon tree boas (Corallus hortulanus), and two Malagasy ground boas (Acrantophis madagascariensis) were subjected to ultrasound imaging with 21 MHz (ball python) and 50 MHz (ball python, Burmese python, Children’s python, Amazon tree boa, Malagasy ground boa) transducers in order to measure the different structures of the anterior segment in clinically normal snake eyes with the aim to review baseline values for clinically important ophthalmic structures. The ultrasonographic measurements included horizontal spectacle diameter, spectacle thickness, depth of sub-spectacular space and corneal thickness. For comparative purposes, a formalin-fixed head of a Burmese python was subjected to micro computed tomography. In all snakes, the spectacle was thinner than the cornea. There was significant difference in spectacle diameter, and spectacle and corneal thickness between the Amazon tree boa and the Burmese and ball pythons. There was no difference in the depth of the sub-spectacular space. The results obtained in the Burmese python with the 50 MHz transducer were similar to the results obtained with micro computed tomography. Images acquired with the 21 MHz transducer included artifacts which may be misinterpreted as ocular structures. Our measurements of the structures in the anterior segment of the eye can serve as orientative values for snakes examined for ocular diseases. In addition, we demonstrated that using a high frequency transducer minimizes the risk of misinterpreting artifacts as ocular structures.

Da Silva M.O., Heegaard S., Wang T., Nyengaard J.R., Bertelsen M.F.

Sabater M., Pérez M.

Ocular and adnexal congenital disorders are those that manifest at birth and could involve single or multiple tissues. Several abnormalities have been reported in literature affecting reptilian ocular and/or adnexal tissues. The objectives of this review are: (i) review those disorders previously reported in reptile literature; (ii) present new cases; (iii) provide a basic classification of them according to the moment of occurrence and (iv) indirectly, encourage the clinician dealing with these cases to go further in their diagnosis. The authors consider that categorizing ocular and adnexal congenital disorders could help the clinician to deal with them. The categorization of these disorders required an intense review of cases previously reported in literature and allows the authors suspect that some of them could not have been accurately diagnosed according to the definitions of the anomalies and/or not accurately described. The authors consider that ocular and adnexal congenital disorders could have been underestimated in reptiles and further studies could be helpful to promote the description of new disorders and to expand the knowledge about those previously reported. The review will first describe abnormalities reported during organogenesis (describing possible etiopathogenesis, cases reported, an approach to their diagnosis and recommended therapeutic options).Then a mention of the ocular disorders occurring after organogenesis is made. These disorders are divided when possible in those affecting all or most part of the globe and those affecting only specific tissues (surface ectoderm, neurocrest and mesenchyma and neuroectoderm).

Liu Y., Ding L., Lei J., Zhao E., Tang Y.

The functioning of the vertebrate eye depends on its absolute size, which is presumably adapted to specific needs. Eye size variation in lidless and spectacled colubrid snakes was investigated, including 839 specimens belonging to 49 genera, 66 species and subspecies. Variations of adult eye diameters (EDs) in both absolute and relative terms between species were correlated with parameters reflecting behavioral ecology. In absolute terms, eye of arboreal species was larger than in terrestrial and semiaquatic species. For diurnal species, EDs of terrestrial species do not differ from semiaquatic species; for nocturnal species the ED of terrestrial species is larger than fossorial species but not different from semiaquatic species. In relative terms, ED did not differ significantly by habitat for diurnal species. Although the ED of terrestrial species is larger than fossorial species there were no differences for nocturnal species between semiaquatic and fossorial snakes. In contrast to other vertebrates studied to date, colubrid EDs in absolute and relative terms are larger in diurnal than in nocturnal species. These observations suggest that among colubrid snakes, eye size variation reflects adaptation to specific habitats, foraging strategies and daily activities, independently of phylogeny.

Lawing A.M., Head J.J., Polly P.D.

Morphological traits that have a functional relationship with the environment can be used to study relationships between organisms and environments through time and across space. Dynamics of the trait-environment complex can be studied with ecometrics in individuals, in populations, and in communities. We explored how closely correlated three skeletal traits are with substrate use, and thus macrohabitat, among communities of snakes with the goal of better understanding how climate and macrovegetation might affect snake assemblages. Substrate use explained a large part of the variance in mean length-to-width ratio of vertebrae (R 2 = 0.66), PC1 of vertebral shape of a mid trunk vertebra (R 2 = 0.46), and relative tail length (R 2 = 0.71). Furthermore, mean relative tail length in snake assemblages across North America is strongly associated with ecoregions and vegetation cover (R 2 = 0.65 and 0.47, respectively). The close relationship with macrovegetation makes relative tail length a useful tool for predicting how snake assemblages will change as climates and biomes change across space or through time. This “ecometric” approach provides a medium-scale link between data collected from ecological studies over decades to data assembled from the fossil record over thousands, tens of thousands, or even millions of years. We show how historical vegetation changes between the early twentieth and twenty-first centuries at five preserves in North America resulted in ecometric changes that parallel the geographic distribution of relative tail length in snake communities across North America.

Williams D.L.

Revell L.J.

Summary 1. Here, I present a new, multifunctional phylogenetics package, phytools, for the R statistical computing environment. 2. The focus of the package is on methods for phylogenetic comparative biology; however, it also includes tools for tree inference, phylogeny input/output, plotting, manipulation and several other tasks. 3. I describe and tabulate the major methods implemented in phytools, and in addition provide some demonstration of its use in the form of two illustrative examples. 4. Finally, I conclude by briefly describing an active web-log that I use to document present and future developments for phytools. I also note other web resources for phylogenetics in the R computational environment.

MENEGON M., DAVENPORT T.R., HOWELL K.M.

A new species of arboreal forest viper (Serpentes: Viperidae: Atheris) from a forest fragment in the Southern Highlands of Tanzania is described and named Atheris matildae sp. nov. The species resembles the forest horned viper, Atheris ceratophora Werner, by bearing horn-like supraciliary scales but it differs in size, body proportions, scalation, scale ultrastructure, and distribution. Genetic divergence is also assessed and the two species have an estimated divergence time of approximately 2.2 million years. An overview of the genus Atheris in Tanzania, including new distribution data, is presented and the conservation status of the new taxon is discussed.

Kaltakci D., Eryilmaz A.

Context is important as a motivational factor for student involvement with physics. The diversity in the types and the functions of animal eyes is an excellent context in which to achieve this goal. There exists a range of subtopics in optics including pinhole, reflection, refraction, and superposition that can be discussed in the context of the animal eye. In addition to ordinary textbook optics questions, the use of context-based questions that model the real world may increase the students' motivation toward optics concepts and their understanding of them. In this article, different optical systems in animal eyes are discussed as a context to teach optics topics with context-based questions.

Veilleux C.C., Lewis R.J.

Many aspects of mammalian visual anatomy vary with activity pattern, reflecting the divergent selective pressures imposed by low light and high light visual environments. However, ambient light intensity can also differ substantially between and within habitats due to differences in foliage density. We explored the effects of interhabitat and intrahabitat variation in light intensity on mammalian visual anatomy. Data on relative cornea size, activity pattern, and habitat type were collected from the literature for 209 terrestrial mammal species. In general, mammalian relative cornea size significantly varied by habitat type. In within-order and across-mammal analyses, diurnal and cathemeral mammals from forested habitats exhibited relatively larger corneas than species from more open habitats, reflecting an adaptation to increase visual sensitivity in forest species. However, in all analyses, we found no habitat-type effect in nocturnal species, suggesting that nocturnal mammals may experience selection to maximize visual sensitivity across all habitats. We also examined whether vertical strata usage affected relative cornea size in anthropoid primates. In most analyses, species occupying lower levels of forests and woodlands did not exhibit relatively larger corneas than species utilizing higher levels. Thus, unlike differences in intensity between habitat types, differences in light intensity between vertical forest strata do not appear to exert a strong selective pressure on visual morphology. These results suggest that terrestrial mammal visual systems reflect specializations for habitat variation in light intensity, and that habitat type as well as activity pattern have influenced mammalian visual evolution.

Kelly C.M., Branch W.R., Broadley D.G., Barker N.P., Villet M.H.

The snake family Lamprophiidae Fitzinger (Serpentes: Elapoidea) is a putatively Late Eocene radiation of nocturnal snakes endemic to the African continent. It incorporates many of the most characteristic and prolific of Africa's non-venomous snake species, including the widespread type genus Lamprophis Fitzinger, 1843 (house snakes). We used approximately 2500 bases of mitochondrial and nuclear DNA sequence data from 28 (41%) of the approximately 68 recognised lamprophiid species in nine of the eleven genera to investigate phylogenetic structure in the family and to inform taxonomy at the generic level. Cytochrome b, ND4 and tRNA gene sequences (mitochondrial) and c-mos sequences (nuclear) were analysed using Maximum Likelihood, Bayesian Inference and Maximum Parsimony methods. The genus Mehelya Csiki, 1903 was paraphyletic with respect to Gonionotophis Boulenger, 1893. To address this, the concept of Gonionotophis is expanded to include all current Mehelya species. The genus Lamprophis emerged polyphyletic: the enigmatic Lamprophis swazicus was sister to Hormonotus modestus from West Africa, and not closely related to its nominal congeners. It is moved to a new monotypic genus (Inyoka gen. nov.). The remaining Lamprophis species occur in three early-diverging lineages. (1) Lamprophis virgatus and the widely distributed Lamprophis fuliginosus species complex (which also includes Lamprophis lineatus and Lamprophis olivaceus) formed a clade for which the generic name Boaedon Duméril, Bibron & Duméril, 1854 is resurrected. (2) The water snakes (Lycodonomorphus) were nested within Lamprophis (sensu lato), sister to Lamprophis inornatus. We transfer this species to the genus Lycodonomorphus Fitzinger, 1843. (3) We restrict Lamprophis (sensu strictissimo) to a small clade of four species endemic to southern Africa: the type species of Lamprophis Fitzinger, 1843 (Lamprophis aurora) plus Lamprophis fiskii, Lamprophis fuscus and Lamprophis guttatus.

El-Bakry A.M.

BRISCHOUX F., PIZZATTO L., SHINE R.

Gower D.J., Hauzman E., Simões B.F., Schott R.K.

Millichamp N.J.

The eyes of snakes are quite unique among vertebrates reflecting their evolutionary history and anatomical differences from other reptiles. Diseases of snake eyes and adnexa are relatively infrequently seen and poorly understood in clinical practice—those conditions encountered can be extremely frustrating to manage due to their anatomical peculiarities.

Ledbetter E.C., Marion J.S., Morrisey J.K.

To describe the surgical repair of traumatic complete spectaculectomy and keratomalacia in a snake.A 10.5-year-old, female, Boelen's python (Simalia boeleni) was presented with iatrogenic, near-complete spectaculectomy associated with bacterial keratitis, keratomalacia, and hypopyon.Corneal samples for cytological evaluation and bacterial culture were collected. Following medical stabilization of the bacterial keratitis, a double-layered dry amniotic membrane graft was placed. The first amniotic membrane layer was placed over the cornea with the edges tucked under the peripheral remnants of the spectacle and secured in place with fibrin glue. The second amniotic membrane layer was placed over the entirety of the spectacle remnant and secured in place with a combination of fibrin glue and sutures. Topical and systemic antimicrobials, topical ophthalmic lubricants, and systemic non-steroidal anti-inflammatory therapy were administered postoperatively.Heterophilic keratitis was identified by cytology and Enterobacter cloacae, Pseudomonas aeruginosa, and Staphylococcus sciuri were cultured from the corneal samples. The amniotic membrane grafts remained in place for several weeks. At 4 months postoperatively, the spectacle was completely regenerated, the subspectacular space restored, and the cornea was transparent. Spectacular vascularization and fibrosis then slowly cleared over the following 6 months.Amniotic membrane grafting with fibrin glue is a relatively simple and effective surgical method to reconstruct extensive defects in the reptilian spectacle and to assist in the management of bacterial keratitis associated with spectacle avulsion.