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RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes.

ABSTRACT: BACKGROUND: Largely because of their direct, negative impacts on human health, the venoms of front-fanged snakes of the families Viperidae and Elapidae have been extensively characterized proteomically, transcriptomically, and pharmacologically. However, relatively little is known about the molecular complexity and evolution of the venoms of rear-fanged colubrid snakes, which are, with a few notable exceptions, regarded as harmless to humans. Many of these snakes have venoms with major effects on their preferred prey, and their venoms are probably as critical to their survival as those of front-fanged elapids and viperids. RESULTS: We sequenced the venom-gland transcriptomes from a specimen of Hypsiglena (Desert Night Snake; family Colubridae, subfamily Dipsadinae) and of Boiga irregularis (Brown Treesnake; family Colubridae, subfamily Colubrinae) and verified the transcriptomic results proteomically by means of high-definition mass spectrometry. We identified nearly 3,000 nontoxin genes for each species. For B. irregularis, we found 108 putative toxin transcripts in 46 clusters with <1% nucleotide divergence, and for Hypsiglena we identified 79 toxin sequences that were grouped into 33 clusters. Comparisons of the venoms revealed divergent venom types, with Hypsiglena possessing a viper-like venom dominated by metalloproteinases, and B. irregularis having a more elapid-like venom, consisting primarily of three-finger toxins. CONCLUSIONS: Despite the difficulty of procuring venom from rear-fanged species, we were able to complete all analyses from a single specimen of each species without pooling venom samples or glands, demonstrating the power of high-definition transcriptomic and proteomic approaches. We found a high level of divergence in the venom types of two colubrids. These two venoms reflected the hemorrhagic/neurotoxic venom dichotomy that broadly characterizes the difference in venom strategies between elapids and viperids.

SUBMITTER: McGivern JJ

PROVIDER: S-EPMC4289226 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes.

McGivern James J JJ Wray Kenneth P KP Margres Mark J MJ Couch Michelle E ME Mackessy Stephen P SP Rokyta Darin R DR

BMC genomics 20141203

<h4>Background</h4>Largely because of their direct, negative impacts on human health, the venoms of front-fanged snakes of the families Viperidae and Elapidae have been extensively characterized proteomically, transcriptomically, and pharmacologically. However, relatively little is known about the molecular complexity and evolution of the venoms of rear-fanged colubrid snakes, which are, with a few notable exceptions, regarded as harmless to humans. Many of these snakes have venoms with major ef ...[more]

PMID: 25476704

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Project description:BackgroundFangs are a putative key innovation that revolutionized prey capture and feeding in snakes, and - along with their associated venom phenotypes - have made snakes perhaps the most medically-significant vertebrate animals. Three snake clades are known for their forward-positioned fangs, and these clades (Elapidae, Viperidae, and Atractaspidinae) contain the majority of snakes that are traditionally considered venomous. However, many other snakes are "rear-fanged": they possess potentially venom-delivering teeth situated at the rear end of the upper jaw. Quantification of fang phenotypes - and especially those of rear-fanged species - has proved challenging or impossible owing to the small size and relative rarity of many such snakes. Consequently, it has been difficult to understand the evolutionary history of both venom and prey-capture strategies across extant snakes. We quantified variation in the dentition of 145 colubriform ("advanced") snake species using microCT scanning and compared dental characters with ecological data on species' diet and prey capture method(s) to understand broader patterns in snake fang evolution.ResultsDental traits such as maxilla length, tooth number, and fang size show strong phylogenetic signal across Colubriformes. We find extreme heterogeneity and evolutionary lability in the rear-fanged phenotype in colubrid (colubrine, dipsadine, and natricine lineages) and lamprophiid snakes, in contrast to relative uniformity in the front fanged phenotypes of other groups (vipers and, to a lesser extent, elapids). Fang size and position are correlated with venom-use in vipers, elapids, and colubrid snakes, with the latter group shifting fangs anteriorly by shortening the entire maxillary bone. We find that maxilla length and tooth number may also be correlated with the evolution of dietary specialization. Finally, an ancestral state reconstruction suggests that fang loss is a recurring phenomenon in colubrid snakes, likely accompanied by shifts in diet and prey capture mode.ConclusionsOur study provides a framework for quantifying the complex morphologies associated with venom use in snakes. Our results suggest that fang phenotypes, and particularly the rear-fanged phenotype, in snakes are both diverse and labile, facilitating a wide range of ecological strategies and contributing to spectacular radiations of these organisms in tropical and subtropical biomes worldwide.

Project description:BackgroundMorphological divergences of snake retinal structure point to complex evolutionary processes and adaptations. The Colubridae family has a remarkable variety of retinal structure that can range from all-cone and all-rod to duplex (cone/rod) retinas. To explore whether nocturnal versus diurnal activity is responsible for constraints on molecular evolution and plays a role in visual opsin spectral tuning of colubrids, we carried out molecular evolution analyses of the visual opsin genes LWS, RH1, and SWS1 from 17 species and performed morphological analyses.ResultsPhylogenetic reconstructions of the RH1 and LWS recovered major clades characterized by primarily diurnal or primarily nocturnal activity patterns, in contrast with the topology for SWS1, which is very similar to the species tree. We found stronger signals of purifying selection along diurnal and nocturnal lineages for RH1 and SWS1, respectively. A blue-shift of the RH1 spectral peak is associated with diurnal habits. Spectral tuning of cone opsins did not differ among diurnal and nocturnal species. Retinas of nocturnal colubrids had many rows of photoreceptor nuclei, with large numbers of rods, labeled by wheat germ agglutinin (WGA), and two types of cones: large cones sensitive to long/medium wavelengths (L/M) and small cones sensitive to ultra-violet/violet wavelengths (UV/VS). In contrast, retinas of diurnal species had only one row of photoreceptor nuclei, with four types of cones: large and double L/M cones, small UV/VS cones, and a second group of small cones, labeled by WGA.ConclusionsFor LWS gene, selection tests did not confirm different constraints related to activity pattern. For SWS1, stronger purifying selection in nocturnal lineages indicates divergent evolutionary pressures related to the activity pattern, and the importance of the short wavelength sensitivity at low light condition. Activity pattern has a clear influence on the signatures of selection and spectral tuning of RH1, with stronger purifying selection in diurnal lineages, which indicates selective pressure to preserve rhodopsin structure and function in pure-cone retinas. We suggest that the presence of four cone types in primarily diurnal colubrids might be related to the gain of color discrimination capacity.

Dataset Information

RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes.

Publications

RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes.

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