Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

Black Bear Reactions to Venomous and Non‐venomous Snakes in Eastern North America

Bears are often considered ecological equivalents of large primates, but the latter often respond with fear, avoidance, and alarm calls to snakes, both venomous and non‐venomous, there is sparse information on how bears respond to snakes. We videotaped or directly observed natural encounters between black bears (Ursus americanus) and snakes. Inside the range of venomous snakes in Arkansas and West Virginia, adolescent and adult black bears reacted fearfully in seven of seven encounters upon becoming aware of venomous and non‐venomous snakes; but in northern Michigan and Minnesota where venomous snakes have been absent for millennia, black bears showed little or no fear in four encounters with non‐venomous snakes of three species. The possible roles of experience and evolution in bear reactions to snakes and vice versa are discussed. In all areas studied, black bears had difficulty to recognize non‐moving snakes by smell or sight. Bears did not react until snakes moved in 11 of 12 encounters with non‐moving timber rattlesnakes (Crotalus horridus) and four species of harmless snakes. However, in additional tests in this study, bears were repulsed by garter snakes that had excreted pungent anal exudates, which may help explain the absence of snakes, both venomous and harmless, in bear diets reported to date.     

Environmental enrichment alters the behavioral profile of ratsnakes (Elaphe)

This study investigated the effects of environmentally enriched and standard laboratory housing conditions on behavioral performance in 16 subadult ratsnakes (Elaphe obsoleta) using a split-clutch design. In a problem-solving task, snakes housed in enriched environments (EC) exhibited shorter latencies to the goal hole as compared to snakes housed in standard conditions (SC). In an open field task, EC snakes tended to habituate more quickly than SC snakes with repeated testing. A feeding task did not reveal any significant differences between EC and SC snakes. A discriminant function analysis correctly assigned all snakes to their appropriate housing treatment groups, based on the responses in each of the behavioral tasks. This suggests that each group had a distinct behavioral profile; that is, EC snakes were more behaviorally adaptive than SC snakes. This study demonstrated that housing conditions can affect the behavior of captive snakes and produce improvements in behavior similar to those seen in mammalian enrichment studies.     

Molecular evolution of the infrared sensory gene TRPA1 in snakes and implications for functional studies

TRPA1 is a calcium ion channel protein recently identified as the infrared receptor in pit organ-containing snakes. Therefore, understanding the molecular evolution of TRPA1 may help to illuminate the origin of "heat vision" in snakes and reveal the molecular mechanism of infrared sensitivity for TRPA1. To this end, we sequenced the infrared sensory gene TRPA1 in 24 snake species, representing nine snake families and multiple non-snake outgroups. We found that TRPA1 is under strong positive selection in the pit-bearing snakes studied, but not in other non-pit snakes and non-snake vertebrates. As a comparison, TRPV1, a gene closely related to TRPA1, was found to be under strong purifying selection in all the species studied, with no difference in the strength of selection between pit-bearing snakes and non-pit snakes. This finding demonstrates that the adaptive evolution of TRPA1 specifically occurred within the pit-bearing snakes and may be related to the functional modification for detecting infrared radiation. In addition, by comparing the TRPA1 protein sequences, we identified 11 amino acid sites that were diverged in pit-bearing snakes but conserved in non-pit snakes and other vertebrates, 21 sites that were diverged only within pit-vipers but conserved in the remaining snakes. These specific amino acid substitutions may be potentially functional important for infrared sensing.     

The snake hiss: potential acoustic mimicry in a viper–colubrid complex

Examples of acoustic Batesian mimicry are scarce, in contrast to visual mimicry. Here we describe a potential case of acoustic mimicry of a venomous viper model by harmless viperine snakes (colubrid). Viperine snakes resemble vipers in size, shape, colour, pattern, and anti‐predatory behaviours, including head flattening, false strikes, and hissing. We sought to investigate whether hissing evolved as part of, or separately to, the viper mimic syndrome. To do this, we recorded and analysed the hissing sounds of several individual asp vipers, viperine snakes, and grass snakes (a close relative of viperine snakes that hisses but does not mimic the asp viper). Frequencies consistently ranged from 40 to 12 000 Hz across species and individuals. All vipers (100%) and most viperine snakes (84%) produced inhalation hissing sounds, in comparison to only 25% of grass snakes. Inhalation hissing sounds lasted longer in vipers than in viperine snakes. The hissing‐sound composition of grass snakes differed significantly from that of both asp vipers and viperine snakes; however, the hissing‐sound composition between viperine snakes and asp vipers was not statistically distinguishable. Whilst grass snake hissing sounds were characterized by high frequencies (5000–10 000 Hz), both vipers and viperine snake hissing sounds were dominated by low frequencies (200–400 Hz). A principal component analysis revealed no overlap between grass snakes and vipers, but important overlaps between viperine snakes and vipers, and between viperine snakes and grass snakes. The likelihood that these overlaps respectively reflect natural selection for Batesian mimicry and phylogeny constraints is discussed. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1107–1114.     

Are Diet Preferences Associated to Skulls Shape Diversification in Xenodontine Snakes?

Snakes are a highly successful group of vertebrates, within great diversity in habitat, diet, and morphology. The unique adaptations for the snake skull for ingesting large prey in more primitive macrostomatan snakes have been well documented. However, subsequent diversification in snake cranial shape in relation to dietary specializations has rarely been studied (e.g. piscivory in natricine snakes). Here we examine a large clade of snakes with a broad spectrum of diet preferences to test if diet preferences are correlated to shape variation in snake skulls. Specifically, we studied the Xenodontinae snakes, a speciose clade of South American snakes, which show a broad range of diets including invertebrates, amphibians, snakes, lizards, and small mammals. We characterized the skull morphology of 19 species of xenodontine snakes using geometric morphometric techniques, and used phylogenetic comparative methods to test the association between diet and skull morphology. Using phylogenetic partial least squares analysis (PPLS) we show that skull morphology is highly associated with diet preferences in xenodontine snakes.     

尖吻蝮人工养殖灌喂技术研究

目的探讨采用灌喂器人工灌喂尖吻蝮技术的可行性。方法采用湖南京湘源蛇类养殖有限公司自主研制的灌喂器人工灌喂尖吻蝮,观察记录随机抽取的30条尖吻蝮幼蛇及30条尖吻蝮成蛇在机器灌喂后每条幼蛇的体重数据,每3个月测量1次,观察12个月统计尖吻蝮的体重增长情况,并与常规灌喂方法饲养的尖吻蝮进行比较。结果灌喂器饲养的尖吻蝮幼蛇成活率为86.67%,平均体重达（482.39±40.19）g;灌喂器饲养的尖吻蝮成蛇成活率为96.67%,平均体重达（1346.13±117.51）g。而同期常规灌喂技术饲养的尖吻蝮幼蛇全部死亡,尖吻蝮成蛇成活率为76.67%,平均体重（878.56±82.39）g。结论人工灌喂器饲养的尖吻蝮幼蛇及成蛇的体重增长快速,成活率高,值得推广。     

Post-translational modification accounts for the presence of varied forms of nerve growth factor in Australian elapid snake venoms

The Australian elapid snakes are amongst the most venomous snakes in the world, but much less is known about the overall venom composition in comparison to Asian and American snakes. We have used a combined approach of cDNA cloning and 2-DE with MS to identify nerve growth factor (NGF) in venoms of the Australian elapid snakes and demonstrate its neurite outgrowth activity. While a single 730 nucleotide ORF, coding for a 243 amino acid precursor protein was detected in all snakes, use of 2-DE identified NGF proteins with considerable variation in molecular size within and between the different snakes. The variation in size can be explained at least in part by N-linked glycosylation. It is possible that these modifications alter the stability, activity and other characteristics of the snake NGFs. Further characterisation is necessary to delineate the function of the individual NGF isoforms.     

湖南主要经济蛇类养殖场的设计与建造调查研究

目的研究出一种适合湖南地域理想的科学经济蛇类人工养殖场。方法采用调查研究法、试验法、归纳总结法等研究方法。结果总结出湖南省经济蛇类养殖场主要有蛇房、露天蛇场、室内外结合蛇场等3种模式,首创了“湖南立体蛇场”模式。结论在湖南省境内采用“湖南立体蛇场”模式进行经济蛇类的养殖效果较好,不仅简单易建、经济合算,而且科学合理、实用方便,达到了预期的目的。     

Snake modulates constriction in response to prey's heartbeat

Many species of snakes use constriction-the act of applying pressure via loops of their trunk-to subdue and kill their prey. Constriction is costly and snakes must therefore constrict their prey just long enough to ensure death. However, it remains unknown how snakes determine when their prey is dead. Here, we demonstrate that boas (Boa constrictor) have the remarkable ability to detect a heartbeat in their prey and, based on this signal, modify the pressure and duration of constriction accordingly. We monitored pressure generated by snakes as they struck and constricted warm cadaveric rats instrumented with a simulated heart. Snakes responded to the beating heart by constricting longer and with greater total pressure than when constricting rats with no heartbeat. When the heart was stopped midway through the constriction, snakes abandoned constriction shortly after the heartbeat ceased. Furthermore, snakes naive to live prey also responded to the simulated heart, suggesting that this behaviour is at least partly innate. These results are an example of how snakes integrate physiological cues from their prey to modulate a complex and ancient behavioural pattern.     

The morphology of the suboccipital region in snakes,and the anatomical and functional diversity of the myodural bridge

The myodural bridge, that is, skeletal muscle fibers attaching to the cervical dura mater, has been described from a variety of mammals and other amniotes. To test an earlier assumption about the presence of the myodural bridge in snakes, a comparative study was designed using a group of Colubrine snakes. Serial histological sections revealed no evidence of the myodural bridge in any of the snakes examined. Further analyses, including histology, computed tomography (CT), and micro-CT imaging of other distantly related snakes, also turned up no evidence of a myodural bridge. The close apposition of adjacent neural arches in snakes may preclude muscle tendons from passing through the intervertebral joint to reach the spinal dura. It is hypothesized that the myodural bridge functions in the clearance of the cerebrospinal fluid (CSF) by creating episodic CSF pressure pulsations, and that snakes are capable of creating equivalent CSF pressure pulsations through vertebral displacement.     

Ontogenetic change in blood oxygen capacity and maximum activity in garter snakes (Thamnophis sirtalis)

Summary There is an ontogenetic increase in the time that garter snakes (Thamnophis s. sirtalis) can maintain maximum activity at 25°C. Newborn snakes are exhausted by 3–5 min of activity while adults can be active for 20–25 min. The increased endurance of adult snakes results from ontogenetic increases in both aerobic and anaerobic energy generation. At rest juvenile and adult snakes have the same whole-body lactic acid concentrations, but at exhaustion adult lactic acid concentrations are 1.5 times those of juveniles. This increase in anaerobic energy production accounts for part of the endurance of adult snakes, but increased aerobic metabolism appears to be more important. Among the mechanisms increasing aerobic metabolism are more effective pulmonary ventilation and a 3-fold ontogenetic increase in blood oxygen capacity.The rapid exhaustion of small garter snakes probably limits the microhabitats they can occupy and the sorts of hunting methods they can employ. Small garter snakes feed only on small prey that are easily subdued. There is an ontogenetic increase in the relative size of prey eaten by garter snakes that parallels the ontogenetic increase in endurance. Adult feeding habits are adopted at the same body size at which adult blood oxygen capacity and endurance are attained.     

Evolution of sex-chromosomes and formation of W-chromatin in snakes

The analysis of sex-chromosome complexes and formation of W-chromatin in 16 species of snakes of the families Boidae, Colubridae, Elapidae, and Hydrophiidae, reveal three very pertinent facts. First, the snakes exhibit various states of the differentiation of the Z and W chromosomes, apparently according to the evolutionary status of the families, being homomorphic in primitive families and well differentiated in highly evolved ones. Second, the demonstration of a heteropycnotic body in the interphase nuclei of the families of a large number of species of snakes has definitely shown that the nuclear sexing is possible not only in those species of snakes where the W chromosome is morphologically distinguishable from the Z, but also in those species where it is not so, but shows an asynchrony in the replicating pattern of W. It is suggested that development of allocycly rather than establishment of structural changes is the first step in the differentiation of the W from the Z in snakes. Third, the absence of coexistence of nucleolus and W-chromatin in a condensed state in the interphase nuclei of different tissues in a few species of snakes reported in this paper suggests that the W-chromatin is responsible for the synthesis of the nucleolus in these snakes.Paper presented at the Third Oxford Chromosome Conference, September, 1970.     

Venom glands and some associated muscles in sea snakes

The venom glands and related muscles of sea snakes conform in their general structure to those of the terrestrial elapids. The venom gland, however, is smaller in size and the accessory gland is considerably reduced. A similar pattern is found in the Australian elapid Notechis. The musculus compressor glandulae is well developed in the sea snakes and in some species its posterior-medial portion runs uninterruptedly from the origin to the insertion of the muscle. This might be considered as a primitive condition suggesting an early divergence of the sea snakes from an ancestral elapid stock. Three species of sea snakes, Aipysurus eydouxi, Emydocephalus annulatus, and E. ijimae, feed on fish eggs and have very small, but still functioning, venom glands. The reduced accessory gland of the sea snakes is apparently connected with their aquatic environment, as a similar condition is found also in the elapine Boulengerina annulata which lives in large lakes of Central Africa. The similarity in structure of the venom gland between sea snakes and Notechis scutatus may point to a possible phylogenetic relationship between this group of Australian elapids and hydrophiine snakes.     

Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico

Seventy-two Mexican garter snakes (Thamnophis eques) and 126 black-bellied garter snakes (T. melanogaster) were collected from 4 localities of the Mesa Central of Mexico between July 1996 and February 1998 and examined for helminths. Both species of garter snakes occurred sympatrically in every locality except in Lake Cuitzeo. Both species of snakes shared 9 helminth species, and in general, T. melanogaster hosted a larger number of species than T. eques. In each locality, a different helminth species showed the highest levels of prevalence and abundance (Spiroxys susanae in Ciénaga de Lerma, Telorchis corti in Lago de Pátzcuaro, Proteocephalus variabilis in Lago de Cuitzeo, and Contracaecum sp. in Lago de Chapala). Helminth communities in garter snakes of the Mesa Central are depauperate and dominated by a single parasite species. In those localities where the snakes occurred in sympatry, helminth communities were, in general, more diverse and species-rich in T. melanogaster. Differences in the ecology and physiology of these species of garter snakes may explain this pattern because black-bellied garter snakes (T. melanogaster) are more aquatic than Mexican garter snakes (T. eques) and primarily eat aquatic prey, potentially exposing themselves to a larger number of helminths transmitted by predator-prey infection. The helminth infracommunities of garter snakes in the Mesa Central of Mexico show a strong Nearctic influence because most of the species infecting these hosts have been recorded in other Nearctic colubrid snakes. However, the helminth infracommunities of these garter snakes are less species-rich and less diverse than those in colubrid snakes in more temperate latitudes. The widespread ecological perturbation of sampling sites in the Mesa Central because of human activity, and geographic differences in foraging ecology of the hosts and, thus, exposure to parasites transmitted by intermediate hosts may help to explain these patterns.     

Snake phylogeny based on osteology,soft anatomy and ecology

Relationships between the major lineages of snakes are assessed based on a phylogenetic analysis of the most extensive phenotypic data set to date (212 osteological, 48 soft anatomical, and three ecological characters). The marine, limbed Cretaceous snakes Pachyrhachis and Haasiophis emerge as the most primitive snakes: characters proposed to unite them with advanced snakes (macrostomatans) are based on unlikely interpretations of contentious elements or are highly variable within snakes. Other basal snakes include madtsoiids and Dinilysia--both large, presumably non-burrowing forms. The inferred relationships within extant snakes are broadly similar to currently accepted views, with scolecophidians (blindsnakes) being the most basal living forms, followed by anilioids (pipesnakes), booids and booid-like groups, acrochordids (filesnakes), and finally colubroids. Important new conclusions include strong support for the monophyly of large constricting snakes (erycines, boines. pythonines), and moderate support for the non-monophyly of the trophidophiids' (dwarf boas). These phylogenetic results are obtained whether varanoid lizards, or amphisbaenians and dibamids, are assumed to be the nearest relatives (outgroups) of snakes, and whether multistate characters are treated as ordered or unordered. Identification of large marine forms, and large surface-active terrestrial forms, as the most primitive snakes contradicts with the widespread view that snakes arose via minute, burrowing ancestors. Furthermore, these basal fossil snakes all have long flexible jaw elements adapted for ingesting large prey ('macrostomy'), suggesting that large gape was primitive for snakes and secondarily reduced in the most basal living foms (scolecophidians and anilioids) in connection with burrowing. This challenges the widespread view that snake evolution has involved progressive, directional elaboration of the jaw apparatus to feed on larger prey.     

Physiological and hormonal control of thermal depression in the tiger snake, Notechis scutatus

Plasma sodium concentrations in field-caught Western tiger snakes, Notechis scutatus, from semi-arid Carnac Island (CI) varied seasonally, with snakes exhibiting significant hypernatraemia during summer and normal concentrations following autumn rain. In contrast, field-caught tiger snakes from a perennial fresh-water swamp (Herdsman Lake, HL) exhibited no significant increase in plasma sodium concentrations during summer. Laboratory-induced hypernatraemia caused thermal depression in both populations; there was a weak negative relationship between plasma sodium concentration and temperature selection that was significant for CI snakes. Hypernatraemia significantly elevated circulating concentrations of the neuropeptide arginine vasotocin (AVT) in both CI and HL snakes. CI snakes injected with a physiological dosage of AVT also evidenced thermal depression. Despite the positive correlation between AVT and both plasma sodium concentration and osmolality for laboratory snakes, field samples from CI snakes indicate that circulating levels of AVT may be influenced more by plasma osmolality than sodium levels. The data suggest that, in CI snakes, chronic dehydration in the field leads to hypernatraemia which may lead to elevated levels of AVT if plasma osmolality also increases. This will in turn invoke a depression in thermal behaviour that may improve the water economy and survival of snakes on semi-arid CI. Although HL snakes do not experience seasonal dehydration, physiological changes away from the stable homeostatic state appear to prompt the same behavioural shifts, illustrating the intrinsic nature of the thermal behaviour in different populations of the same species of snake.     

COLOR-PATTERN VARIATION IN LAKE ERIE WATER SNAKES: PREDICTION AND MEASUREMENT OF NATURAL SELECTION

A classic example of natural selection, that of color-pattern variation in Lake Erie island populations of water snakes, was reexamined to overcome shortcomings resulting from classification of snakes into discrete color-pattern categories and use of cross-sectional data. Four continuously varying color-pattern components (DB, the number of dorsal blotches; LB, the number of lateral blotches; ROWS, the height of lateral blotches measured in scale rows; and VEXT, the extent of ventral pigmentation) were analyzed. Patterns of natural selection were predicted from the relationship between color-pattern scores and independent measures of relative crypsis. Tests for natural selection were carried out using longitudinal data on neonate to juvenile-aged snakes and cross-sectional data on juvenile to adult-aged snakes. As predicted, the form of selection differed between younger and older age classes of snakes: selection resulted in a reduction in DB and LB among neonate and juvenile snakes but had little influence on color-pattern components in older snakes. The correspondence between observed patterns of natural selection and predictions based on the relationship between color-pattern scores and relative crypsis supports the hypothesis that differential predation by visual predators on younger age classes of snakes is the mechanism of selection. Gene flow from mainland populations or the initial lack of an allele necessary for reduced pattern may explain why selection has not resulted in greater differentiation between island and mainland populations.     

Cytogenetics of the Javan file snake (Acrochordus javanicus) and the evolution of snake sex chromosomes

Advanced snakes (Caenophidia) are an important group including around 90% of the recent species of snakes. The basal splitting of the clade is still rather controversial, and it is not fully understood when the differentiation of sex chromosomes started in snake evolution. To help resolve these questions, we performed cytogenetic analysis on the Javan file snake, also known as the elephant trunk snake (Acrochordus javanicus) from the family Acrochordidae, which occupies an informative phylogenetic position. For the first time for acrochordids, we identified heteromorphic ZZ/ZW sex chromosomes with a highly heterochromatic W chromosome. These traits are likely synapomorphies of advanced snakes. In contrast to other caenophidian snakes, the Javan file snake lacks an accumulation of Bkm repeats and interstitial telomeric repeats on the W chromosome. This observation supports the sister group relationship between acrochordids and all other caenophidian snakes including the family Xenodermatidae and questions the suggested role of Bkm repeats in the formation of sex heterochromatin in snakes. The revealed partial gene content of the Z chromosome in acrochordids supports the hypothesis that the progressive degeneration of the W chromosome commenced in snakes before the basal split of Caenophidia, albeit its evolutionary rate in file snakes might be slower than in their sister lineage.