Evolution of the eyes of vipers with and without infrared-sensing pit organs

Gower, David J.; Sampaio, Filipa L.; Peichl, Leo; Wagner, H; Loew, Ellis R.; McLamb, William Troy; Douglas, R. H.; Orlov, Nikolai L.; Grace, Michael S.; Hart, Nathan S.; Hunt, David M.; Partridge, Julian C.; Simões, Bruno F.

doi:10.1093/biolinnean/blz003

Cited by 26 publications

(42 citation statements)

References 101 publications

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“…Regarding photopigment spectral sensitivities, all the predicted and experimentally demonstrated (by MSP) values for LWS-expressing cones were close to 553-555 nm (Simões et al, 2016a;Katti et al, 2018;Bittencourt et al, 2019;Gower et al, 2019). Interestingly, Gower et al (2019) measured a spectral peak near 554 nm for the LWS photopigment for one viperine and one crotaline (A. contortrix, B. arietans), whereas this photopigment was blue-shifted to 541 nm for a different crotaline, C. atrox; however the tuning mechanisms were not investigated in detail.…”

Section: Ophidia (Snakes)mentioning

confidence: 53%

“…Snakes in general terms can be separated into Scolecophidia (blindsnakes and wormsnakes), Henophidia (boas, pythons and reatives), and Caenophidia (all other snakes), and in many ways these three groups have distinct visual systems. No snake possesses more than three of the possible five opsin classes expressed in reptiles, specifically LWS, SWS1, and RH1 (Davies et al, 2009;Hauzman et al, 2014Hauzman et al, , 2017Simões et al, 2015Simões et al, , 2016aSchott et al, 2016;Bhattacharyya et al, 2017;Katti et al, 2018;Bittencourt et al, 2019;Gower et al, 2019). The first snake visual opsin genes to be sequenced were by Davies et al (2009) in the henophidian royal python (Python regius) and sunbeam snake (Xenopeltis unicolor).…”

Section: Ophidia (Snakes)mentioning

confidence: 99%

“…The first snake visual opsin genes to be sequenced were by Davies et al (2009) in the henophidian royal python (Python regius) and sunbeam snake (Xenopeltis unicolor). Most snakes possess UV-sensitive (360 nm) and LWS (around 550 nm) cones, suggesting they are dichromatic (Sillman et al, 1999(Sillman et al, , 2001Davies et al, 2009;Katti et al, 2018;Bittencourt et al, 2019;Gower et al, 2019). However, with little overlap in the spectra of these photopigments, it would be predicted that snakes are generally colorblind due to photoreceptor opponency (Michael, 1966;Hemmi et al, 2002).…”

Section: Ophidia (Snakes)mentioning

confidence: 99%

“…The visual system of viperid caenophidians has been investigated in detail in a few recent studies (Simões et al, 2016a;Katti et al, 2018;Bittencourt et al, 2019;Gower et al, 2019). Simões et al (2016a) obtained partial sequences of visual opsin genes expressed in three African vipers (Echis ocellatus, Causus rhombeatus, and Bitis nasicornis), Katti et al (2018) and Bittencourt et al (2019) generated homologous sequences from South American vipers (Bothrops atrox, Bothrops jararaca, and Crotalus durissus terrificus), and Gower et al (2019) sampled vipers from different continents including some of those previously studied (i.e., Azemiops kharini, Bothriechis schlegelii, Trimeresurus trigonocephalus, Vipera berus, Agkistrodon contortrix, Bitis arietans, Cerastes cerastes, Crotalus durissus, Echis coloratus, and Crotalus atrox).…”

Section: Ophidia (Snakes)mentioning

confidence: 99%

“…recently by Simões and Gower (2017), many studies have been published since that publication, primarily investigating the visual system of snakes (Bhattacharyya et al, 2017;Hauzman et al, 2017;Katti et al, 2018;Schott et al, 2018;Bittencourt et al, 2019;Gower et al, 2019;among others); thus shedding more light on the visual system and the activity patterns of these animals. In addition, this review forms part of a special Research (Themed) Topic ("Multiplicity of physiological systems that detect light or are regulated by photic information").…”

Section: Introductionmentioning

confidence: 99%

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The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

2019

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Reptiles are a highly diverse class that consists of snakes, geckos, iguanid lizards, and chameleons among others. Given their unique phylogenetic position in relation to both birds and mammals, reptiles are interesting animal models with which to decipher the evolution of vertebrate photopigments (opsin protein plus a light-sensitive retinal chromophore) and their contribution to vision. Reptiles possess different types of retinae that are defined primarily by variations in photoreceptor morphology, which range from pure-cone to rod-dominated retinae with many species possessing duplex (rods and cones) retinae. In most cases, the type of retina is thought to reflect both the lifestyle and the behavior of the animal, which can vary between diurnal, nocturnal, or crepuscular behavioral activities. Reptiles, and in particular geckos and snakes, have been used as prime examples for the "transmutation" hypothesis proposed by Walls in the 1930s-1940s, which postulates that some reptilian species have migrated from diurnality to nocturnality, before subsequently returning to diurnal activities once again. This theory further states that these behavioral changes are reflected in subsequent changes in photoreceptor morphology and function from cones to rods, with a return to cone-like photoreceptors once again. Modern sequencing techniques have further investigated the "transmutation" hypothesis by using molecular biology to study the phototransduction cascades of rod-and cone-like photoreceptors in the reptilian retina. This review will discuss what is currently known about the evolution of opsin-based photopigments in reptiles, relating habitat to photoreceptor morphology, as well as opsin and phototransduction cascade gene expression.

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Section: Ophidia (Snakes)mentioning

confidence: 53%

Section: Ophidia (Snakes)mentioning

confidence: 99%

Section: Ophidia (Snakes)mentioning

confidence: 99%

Section: Ophidia (Snakes)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

2019

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Embryonic development and cranial ossification of the Japanese Aodaishō, Elaphe climacophora (Serpentes: Colubridae): with special reference to the prootic bone and auditory evolution in snakes

Nojiri,

Werneburg,

Sakai

et al. 2024

The Anatomical Record

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Snakes show remarkably deviated “body plan” from other squamate reptiles. In addition to limb loss, they have accomplished enormous anatomical specialization of the skull associated with the pit organs and the reduction of the tympanic membranes and auditory canals in the outer ears. Despite being the most diverse group of snakes, our knowledge of the embryonic staging for organogenesis and cranial ossification has been minimal for Colubridae. Therefore, in the present observation, we provide the first embryonic description of the Japanese rat snake Elaphe climacophora. We based our study on the Standard Event System (SES) for external anatomical characters and on a description of the cranial ossification during post‐ovipositional development. We further estimated the relative ossification timing of each cranial bony element and compared it with that of selected other snakes, lizards, turtles, and crocodilians. The present study shows that the relative ossification timing of the palatine and pterygoid bones is relatively early in squamates when compared to other reptiles, implying the developmental integration as the palate–pterygoid complex in this clade and functional demands for the unique feeding adaptation to swallow large prey with the help of their large palatine and pterygoid teeth. Furthermore, unlike in species with pit organs, the prootic bone of Ela. climacophora is expanded to provide articulation with the supratemporal, thereby contributing to the hearing system by detecting substrate vibration. We also demonstrate that the relative timing of the prootic ossification is significantly accelerated in colubrids compared to snakes with pit organs. Our finding suggests that the temporal changes of the prootic ossification underpin the evolution of the perception of the ground‐bourne sound signals among snakes.

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Patterns of morphological variation and ecological correlates in the skull of vipers (Serpentes: Viperidae)

Carrasco,

Prystupczuk,

Koch

et al. 2023

Journal of Morphology

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The skull of vipers is a highly kinetic anatomical structure involved in envenomating and consuming of prey. Morphological knowledge about the viperid skull is based on studies on some groups of species, but information on its variation within the whole family and its functional morphology is still scarce. In this study, we aimed to explore variation in skull morphology among species of the three subfamilies of Viperidae, and test whether that variation correlates with macrohabitat and diet. We performed quantitative analyses of the viperid skull based on broad taxonomic sampling and two methodological approaches: linear and geometric morphometrics. The results of both approaches showed that much of the variation lies in differences of shape and relative size of the premaxilla, the nasals, the frontals, and the parietals. The results indicated that phylogeny and size influence the shape of the skull, but we also found evidence of morphological differentiation between arboreal and terrestrial species and in species with mammal specialist diet. Our findings imply that, besides evolutionary allometry and phylogenetic signal, demands of particular diets coupled with use of certain habitats have in part shaped morphological evolution of the viperid skull.

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Evolution of the eyes of vipers with and without infrared-sensing pit organs

Cited by 26 publications

References 101 publications

The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

The Diversity and Adaptive Evolution of Visual Photopigments in Reptiles

Embryonic development and cranial ossification of the Japanese Aodaishō, Elaphe climacophora (Serpentes: Colubridae): with special reference to the prootic bone and auditory evolution in snakes

Patterns of morphological variation and ecological correlates in the skull of vipers (Serpentes: Viperidae)

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