Friday, December 9, 2016

The Frilled Lizard and its phylogeography

A typical defensive display of a Frilled Lizard.
The savanna-dwelling Australo-Papuan Frilled Lizards' spectacular threat display has made the lizard world famous. They are distributed across northern Australia and southern New Guinea. In a recent  Molecular Phylogenetics and Evolution article Pepper and colleagues (2017) examine the Frilled Lizard's phylogeography as it relates to changes in the savanna vegetation in the Plio/Pleistocene and the associated increase in aridity. The authors generated sequence data for one mitochondrial and four nuclear DNA loci (5052 base pairs) for 83 frilled lizards sampled throughout their range. They also quantified body proportion variation for 279 individuals. Phylogenetic analyses based on maximum likelihood and Bayesian species-tree methods resulted in three shallow clades that replace each other across the monsoon tropics. They found the expected pattern of male biased sexual size dimorphism in both maximum body size and head size but there was no sexual dimorphism in overall body shape or in frill size, relative to head size, supporting the hypothesis that the frill is used primarily as a threat display rather than a sexual display. The genetic clades are broadly consistent with known clinal variation in frill color that gradually shifts from west to east (red, orange, yellow/white) but otherwise show little morphological differentiation in body proportion measures. The biogeographic breaks between clades occur at the Carpentaria Gap and the lowlands surrounding the Ord River. Ecological niche modeling predicts where habitat suitability for Frilled Lizards in these regions. Extremely low intra-clade genetic diversity over vast geographic areas is indicative of recent gene flow that would likely have been facilitated by widespread savanna during interglacials, Or alternatively, may reflect population bottlenecks induced by extreme aridity during Pleistocene glacials. The shallow divergence between Australian and New Guinean samples is consistent with recent connections between Australia and New Guinea that would have been  via a savanna corridor across the Torres Strait. The authors do not support taxonomic recognition of any of the frilled lizard clades and consider C. kingii a single species with shallow phylogeographic structure and clinal variation in frill color.

Citation
Pepper M, Hamilton DG, Merkling T, Svedin N, Cser B, Catullo RA, Pryke SR, Keogh JS. Phylogeographic structure across one of the largest intact tropical savannahs: Molecular and morphological analysis of Australia’s iconic frilled lizard Chlamydosaurus kingii. 2017. Molecular Phylogenetics and Evolution. 106:217-27.

Thursday, December 8, 2016

Fossil Miocene amphibians and reptiles from Plakias, Crete


A modern alytid European frog, Bombina. JCM
The Neogene (the Miocene and Pliocene) extends from about 22.5 to 2.5 million years ago, and it has been termed "the age of snakes."  The global climate became seasonal, drier and cooler. Polar ice caps formed and thickened, and by the end of the Neogene the first of a series of glaciations of the current Ice Age began. Both the marine and continental flora and fauna contained modern looking species. Many older lineages of amphibians and reptiles had disappeared and were replaced by more modern lineages. Birds and mammals continued to dominant terrestrial vertebrate communities, and the first hominids, the ancestors of humans, evolved in Africa and dispersed into Eurasia. The Miocene composed the bulk of this time segment of Earth's history. In a new paper published in Geobios, Georgalis et al (2016) report on the fossil amphibian and reptiles from the late Miocene of Crete.

The excavation site was at Plakias (early Tortonian, MN 9), Crete, Greece. Most of the material recovered was fragmentary and precludes precise taxonomic assignment. However, the herpetofauna of Plakias was diverse and composed at least six different taxa: an alytid frog, a crocodilian, two turtles (a pan-trionychid and a geoemydid) and two squamates (an amphisbaenian and a colubroid snake). The crocodilian material represents the first such fossils described from Greece and furthermore, one of the latest occurrences of this group in Europe. The pan-trionychid and the geoemydid represent the oldest occurrences of these groups in Greece and further add to their scarce Miocene record from this country. The first description of a fossil amphisbaenian from Greece is also provided. The new specimens from Plakias add to our knowledge of the Miocene herpetofaunas of southeastern Europe. The single colubroid snake specimen adds further to the published record of Miocene snakes from Greece, whereas the amphisbaenian vertebra from Plakias represents the first described fossil of this group from the country, suggesting that amphisbaenians had a continuous range in the northern Mediterranean area.


Citation
Georgalis, G.L., Villa, A., Vlachos, E. and Delfino, M., 2016. Fossil amphibians and reptiles from Plakias, Crete: A glimpse into the earliest late Miocene herpetofaunas of southeastern Europe. Geobios.

Wednesday, December 7, 2016

Impact of food on an ambush specialist - the Puff Adder

The puff adder, Bitis arietans.
The effect of food availability on the spatial ecology of snakes  is under studied. Snake are low-energy specialists, particularly species that specialize in ambush foraging.  Ambush specialists can feed infrequently and  endure long periods without food. Because they have low-energy requirements, one possible tactic for feeding may be to simply ambush for longer periods when prey availability is low, and decrease the potential costs associated with locating new ambush sites. In a forthcoming paper Glaudas and Alexander  (2017) used radiotelemetry, supplemental feeding, and remote video cameras on free-ranging male puff adders (Bitis arietans) in South Africa to test the hypothesis that food intake affects the foraging ecology of extreme low-energy, ambush foragers. They also quantified their natural feeding rates. Supplementally fed puff adders improved their body condition, spent less time foraging, and decreased distance traveled compared to control snakes. However, movement frequency and home range size did not differ between the two groups. These findings indicate that control snakes traveled farther within similar-sized home ranges compared to fed snakes and did so at no survival cost. Further, naturally foraging puff adders successfully caught a prey of small size once every 10 days on average. Hence, despite their “sit-and-wait” foraging strategy and their low-energy intake/requirements, underfed puff adders travel widely to presumably find appropriate ambush sites that maximize prey capture. This study provides the first strong evidence that the spatial activity of a terrestrial vertebrate species with extremely low energetic demands is significantly affected by
food intake.

Citation

Glaudas X, Alexander GJ. 2017. Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake. Behavioral Ecology and Sociobiology. 71(1):5.

Galapagos Land Iguana - seed dispersal agent

A Galápagos Land Iguana (Conolophus subcristatus).
Photo credit Traveset et al.
The isolation of ocean islands like the Galápagos prevents the arrival of large mammals, which disperse the seeds of many plants by ingesting them. In the absence of mammals, this function is filled by birds, tortoises, lizards and iguanas. To date, no investigation had been carried out into the role iguanas play with at least ten species of plants.

The survival of many native and introduced plants depends in part on the role of animals in pollination and seed dispersal. The ingestion and subsequent expulsion of seeds in animal faeces means a proportion of them return to the soil at a more distant location.

In addition to birds, the Galápagos giant tortoise is the animal that disperses most of seeds over great distances on the islands, followed by the endemic land iguanas, of which there are three species which feed on fruit and vegetation near ground level, as they do not climb. However apart from anecdotal records, their potential for seed dispersal had not to date been confirmed.

A study published in the journal 'Integrative Zoology' demonstrates for the first time how by dispersing seeds, the Galápagos land iguana (Conolophus subcristatus) contributes to the survival of indigenous and introduced plants plant species on Fernandina Island, which covers 642 km2 of land.

"We knew that female iguanas on this island cover large distances, around 10 kilometres, and climb up to 1,500 metres of altitude to lay their eggs at the island's volcanic crater," Anna Traveset from the Mediterranean Institute for Advanced Studies (CSIC-UIB), the lead author of the study, outlines.

Between February 2010 and 2011, the researchers collected 160 faeces samples, in which they identified 5,705 seeds from 32 plant species. According to the team, at least 80% of the seeds (around 4,545) were damaged.

With the remaining seeds, which remained intact after passing through the reptile's intestines, the team ran an experiment in which they planted 849 seeds from 29 plant species; only around 4% of these were germinated over 200 days later.

"Considering the local abundance of land iguanas and the large amount of seeds ingested by these animals, even if only a small proportion germinates, they can be considered important for plant dissemination to new areas in this young island," Traveset writes in the article.

In fact, some plants appear to benefit greatly from this action. According to the paper, 63% of the seeds belonged to native plants, a third of which were endemic to the Galápagos Islands. Six per cent were from introduced species and the remainder (31%) could not be identified.

Citation
Traveset A, Nogales M, Vargas, Rumeu B, Olesen JM, Jaramillo P, Heleno R. 2016. Galápagos land iguana (Conolophus subcristatus) as a seed disperser. Integrative Zoology, 2016; 11 (3): 207 DOI: 10.1111/1749-4877.12187

Friday, November 11, 2016

Three new species in the Tegu teguixin Group

The Cryptic Golden Tegu, Tupinambis cryptus,one of the newly 
described species. Tob is an adult from Trinidad middle
 is a juvenile from Tobago. Bottom is a female on a termite nest,
 probably looking of a place to deposit her eggs. JCM, Graham White.
The golden tegu lizard, previously thought to be a single species, may actually comprise four distinct clades, including three new cryptic species, according to a study published August 3, 2016 in the open-access journal PLOS ONE by John Murphy from the Field Museum of Natural History, USA and colleagues.

Tegus are among the largest Neotropical lizards, and while some species occur only in Brazil, Tupinambis teguixin inhabits much of northern South America. Commonly known as the golden tegu, T. teguixin is also sometimes called the "black and white" tegu and can be confused with the closely related species, Salvator merianae. To help resolve the systematics and nomenclature of this species, the authors examined museum samples of golden tegus for genetic and morphological differences across its geographical distribution. The authors noted subtle differences in leg scale morphology, as well as the shape of eye and lip areas, and identified substantial genetic divergence across the tegus large range.

The authors split the species currently recognized as T. teguixin into four morphologically distinct but geographically overlapping species, including three new cryptic species -- T. cryptus, T. cuzcoensis, and T. zuliensis -- that look similar to the human eye but are genetically distinct. The authors suggest that further research in northeastern South America might identify additional species within the T. teguixin group, which would aid in planning for tegu conservation.

"We demonstrate for the first time that two lineages of the Golden Tegu,Tupinambis teguixin, are living side by side at multiple locations in South America, and that T. teguixin is composed of at least four distinct species," said John Murphy. "This situation is known in many other species. What is surprising is that it has gone unrecognized in a species heavily exploited by humans for more than 200 years."
Citation
John C. Murphy, Michael J. Jowers, Richard M. Lehtinen, Stevland P. Charles, Guarino R. Colli, Ayrton K. Peres, Catriona R. Hendry, R. Alexander Pyron. Cryptic, Sympatric Diversity in Tegu Lizards of the Tupinambis teguixin Group (Squamata, Sauria, Teiidae) and the Description of Three New Species. PLOS ONE, 2016; 11 (8): e0158542 DOI: 10.1371/journal.pone.0158542

A re-evaluation of the four-legged snake Tetrapodophis amplectus

Reconstruction of Tetrapodophis.
In 2015, Martill et al. described Tetrapodophis amplectus, a fossil snake with four legs. Tetrapodophis was found in the Bürgermeister-Müller-Museum, a natural history museum in Solnhofen, Germany, while students were on a field trip to the museum.  The Brazilian fossil was part of an exhibit on the Cretaceous and estimated to be 110 million years old. The fossil was part of a larger exhibition on Cretaceous fossils.
The snake, was 20 cm from head to toe, although it may have grown much larger. The head is the size of an adult fingernail, and the smallest tail bone is only a quarter of a millimeter long. But the most remarkable thing about it is the presence of four limbs each ending in digits. The front legs are about 1cm long. The back legs are slightly longer and the feet are larger than the hands. The authors hypothesized that they may have been used to grasp prey or mates. The fossil Tetrapodophis apparently had food in its guts when it was preserved, the remains appeared to be from a salamander.
The authors considered Tetraphodophis a snake, not a lizard because of the elongated body; the tooth implantation, the direction of the teeth, and the pattern of the teeth and the bones of the lower jaw are all snake-like. The fossil also suggests a single row of ventral scales.
In the same issue of Science, Evans (2015) notes that snakelike bodies evolved at least 26 times in squamates and that body elongation is always correlated with limb reduction and that the forelimbs are usually lost first. She also observed that the threshold body length at which limb reduction begins is about 70 body vertebrae (or precaudal vertebrae). Tetrapodophis is remarkable in having about 160 precaudal vertebrae and retaining its anterior limbs. Evans also notes Tetrapodophis is like lizards in having distinct vertebral regions of the vertebral column.  It has 10 or 11 short-ribbed neck vertebrae adjacent to the tiny forelimbs. Some generalized terrestrial lizards and a neck of about this same length. Thus, as in long-bodied lizards, elongation of the snake skeleton occurred in the trunk region and not the neck. If Tetrapodophis is indeed a stem-snake, then body elongation preceded loss of the forelimbs.
In second look at the fossil by Lee et al. (2016) suggests Tetrapodophis may not, in fact be a snake at all. Instead they suggest it may be a dolichosaurid, a Cretaceous four-legged marine lizard with an elongated, snake-like body.
Tetrapodophis lacks characters that would be expected in a snake, including re-curved teeth. Lee and colleagues reevaluated the ecomorphology of this fossil using a multivariate morphometric analysis and reexamination of the limb anatomy. Their analysis suggests that the body proportions are unusual and similar to both burrowing and surface-active squamates. They also show it exhibits enlarged first metapodials and reduced tarsal-carpal ossification. These traits imply Tetrapodophis was aquatic.
Unfortunately, the fossil is privately owned and after Lee’s team took photos and measurements, the specimen was removed from the museum so that it can no longer be studied.  

Citations
Evans S. 2016. Four legs too many? Science. 349(6246):374-5.

Lee MS, Palci A, Jones ME, Caldwell MW, Holmes JD, Reisz RR. 2016. Aquatic adaptations in the four limbs of the snake-like reptile Tetrapodophis from the Lower Cretaceous of Brazil. Cretaceous Research. 30, 66:194-199.

Martill DM, Tischlinger H. Longrich NR 2015. A four-legged snake from the Early Cretaceous of Gondwana. Science, 349(6246): 416-419.


Wednesday, October 26, 2016

A new toxin from the Blue Coral Snake

(a) Specimen of Calliophis bivirgatus, the blue coral
snake (Photo by Tom Charlton). (b) Dissected preserved 
112 cm Calliophis bivirgatus specimen with 29 cm elongated 
venom glands (arrows).
The Asian Coral snakes in the genus Calliophis feed upon other snakes, including other snake-eating venomous species of Elapidae such as kraits (Bungarus) and king cobras (Ophiophagus). A unique evolutionary scenario ensues, a chemical arms race between predator and prey in which the risk of role reversal becomes a key selection pressure driving the evolution of toxins that rapidly render prey incapable of retaliation or escape. Snakes that hunt animals capable of inflicting serious retaliatory wounds often release their intended prey after envenomation. In this situation, selection may favour the evolution of toxins that rapidly disable prey, either to prevent it moving too far to be recovered or to prevent the possibility of it attacking and injuring the snake.

With its combination of electric blue dorsolateral stripes and neon red head, tail, and ventral scales, the blue coral snake, Calliophis bivirgatus, is arguably one of the world’s most striking species of snake. An encounter with one is high on the list for many reptile enthusiasts and nature photographers visiting southern Thailand, Malaysia, Singapore, and western Indonesia. The species is of additional interest to anatomists and toxinologists studying the evolution and diversification of the snake venom system as it (along with its congener C. intestinalis) possesses novel elongated venom glands that extend up to one quarter of the length of its body. It is also of medical significance as, in spite of only a small handful of confirmed bites, it has been responsible for at least one human fatality, is suspected of causing at least one more, and has no known antivenom. In spite of these high levels of interest, the venom has been subject to relatively few studies. Studies that examined the toxin content of the venom concluded that all the three-finger toxins present were exclusively cytotoxic in their effects. However, this limited scope of activity attributed to the venom was reflective of the very narrow scope of assays performed and cytotoxicity was largely assumed based on similarity of partial sequences to other toxin types from other snakes rather than full activity characterisation. One study, which examined the usefulness of Taiwan antivenom, preincubated the venom with antivenom (a clinically unrealistic situation) and even then required very high doses to exert any meaningful level of inhibition.

In a new paper Yang et al. (2016) show that the venom is unique in producing spastic paralysis, in contrast to the flaccid paralysis typically produced by neurotoxic snake venoms. The toxin responsible, is named calliotoxin (δ-elapitoxin-Cb1a), a three-finger toxin (3FTx). The calliotoxin molecule has a form of neurotoxicity, previously known from cone snail and scorpion venoms, and is identified for the first time from the venom of a snake. Calliotoxin shifts the voltage-dependence of NaV1.4 activation to more hyperpolarised potentials, inhibits inactivation, and produces large ramp currents, consistent with its profound effects on contractile force in an isolated skeletal muscle preparation. Voltage-gated sodium channels (NaV) are a particularly attractive pharmacological target as they are involved in almost all physiological processes including action potential generation and conduction. Accordingly, venom peptides that interfere with NaV function provide a key defensive and predatory advantage to a range of invertebrate venomous species including cone snails, scorpions, spiders, and anemones. Enhanced activation or delayed inactivation of sodium channels by toxins is associated with the extremely rapid onset of tetanic/excitatory paralysis in envenomed prey animals. A strong selection pressure exists for the evolution of such toxins where there is a high chance of prey escape. However, despite their prevalence in other venomous species, toxins causing delay of sodium channel inhibition have never previously been described in vertebrate venoms. Here we show that NaV modulators, convergent with those of invertebrates, have evolved in the venom of the long-glanded coral snake. Calliotoxin represents a functionally novel class of 3FTx and a structurally novel class of NaV toxins that will provide significant insights into the pharmacology and physiology of NaV. The toxin represents a remarkable case of functional convergence between invertebrate and vertebrate venom systems in response to similar selection pressures. These results underscore the dynamic evolution of the Toxicofera reptile system and reinforces the value of using evolution as a roadmap for biodiscovery.

Citation
Yang DC, Deuis JR, Dashevsky D, Dobson J, Jackson TN, Brust A, Xie B, Koludarov I, Debono J, Hendrikx I, Hodgson WC. 2016. The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus). Toxins. 8(10):303.

Monday, October 24, 2016

Loss and Re-emergence of Legs in Snakes


This image depicts mouse embryos with the ZRS from cobra or 
python inserted into their genomes, replacing the normal gene regulator. 
Their truncated limb development is visible in the comparative 
bone scans. Credit: Kvon et al. Cell 2016
Snakes lost their limbs over 100 million years ago, but scientists have struggled to identify the genetic changes involved. A Cell paper publishing October 20 sheds some light on the process, describing a stretch of DNA involved in limb formation that is mutated in snakes. When researchers inserted the snake DNA into mice, the animals developed truncated limbs, suggesting that a critical stretch of DNA lost its ability to support limb growth during snake evolution.

"This is one of many components of the DNA instructions needed for making limbs in humans and, essentially, all other legged vertebrates. In snakes, it's broken," says Axel Visel, a geneticist at the Lawrence Berkeley National Laboratory and senior author on the paper. "It's probably one of several evolutionary steps that occurred in snakes, which, unlike most mammals and reptiles, can no longer form limbs."

Today's serpents have undergone one of the most dramatic body plan changes in the evolution of vertebrates. To study the molecular roots of this adaptation, Visel and his colleagues started looking at published snake genomes, including the genomes from basal snakes such as boa and python, which have vestigial legs -- tiny leg bones buried in their muscles -- and advanced snakes, such as viper and cobra, which that have lost all limb structures. Within these genomes, they focused specifically on a gene called Sonic hedgehog, or Shh, involved in many developmental processes -- including limb formation. The researchers delved further into one of the Shh gene regulators, a stretch of DNA called ZRS (the Zone of Polarizing Activity Regulatory Sequence) that was present but had diverged in snakes.

To determine the consequences of these mutations, the researchers used CRISPR, a genome-editing method, to insert the ZRS from various other vertebrates into mice, replacing the mouse regulator. With the ZRS of other mammals, such as humans, the mice developed normal limbs. Even when they inserted the ZRS from fish, whose fins are structurally very different from limbs, the mice developed normal limbs. However, when the researchers replaced the mouse ZRS with the python or cobra version, the mice went on to develop severely truncated forelimbs and hindlimbs.

"Using these new genomic tools, we can begin to explore how different evolutionary versions of the same enhancer affect limb development and actually see what happens," says Visel. "We used to be mostly staring at sequences and speculating about molecular evolution, but now, we can really take these studies to the next level."

To identify the mutations in the snakes' ZRS that were responsible for its inactivation during snake evolution, the researchers took a closer look at the evolutionary history of individual sequence changes. By comparing the genomes of snakes and other vertebrates, they identified one particularly suspicious 17 base-pair deletion that only occurred in snakes; this deletion removed a stretch of the ZRS that has a key role in regulating the Shh gene in legged animals.

The research team turned back the evolutionary clock, restoring the missing 17 base pairs in an artificially created hybrid version of the python ZRS, and tested the edited DNA in mice. Those that carried this evolutionarily "resurrected" ZRS in their genome, replacing their normal regulator, developed normal legs. However, Visel cautions that the evolutionary events were probably more complex than just the one deletion: "There's likely some redundancy built into in the mouse ZRS. A few of the other mutations in the snake ZRS probably also played a role in its loss of function during evolution."

Of course, snakes aren't the only vertebrate animals that lack arms and legs -- some lizards, eels and other fish, and marine mammals, for example, have also adapted limb reduction to varying degrees and likely underwent a slightly different evolutionary process. "Loss of limbs has occurred multiple times independently during animal evolution, and it's safe to assume that mutations affecting other genes were involved," says Visel. "It's a complex problem, but with the introduction of genome-editing tools, we can finally start tying specific DNA changes to alterations in body shape more systematically."

Citations
Evgeny Z. Kvon, Olga K. Kamneva, Uirá S. Melo, Iros Barozzi, Marco Osterwalder, Brandon J. Mannion, Virginie Tissières, Catherine S. Pickle, Ingrid Plajzer-Frick, Elizabeth A. Lee, Momoe Kato, Tyler H. Garvin, Jennifer A. Akiyama, Veena Afzal, Javier Lopez-Rios, Edward M. Rubin, Diane E. Dickel, Len A. Pennacchio, Axel Visel. Progressive Loss of Function in a Limb Enhancer during Snake Evolution. Cell, 2016; 167 (3): 633 DOI: 10.1016/j.cell.2016.09.028

Francisca Leal, Martin J. Cohn. Loss and Re-emergence of Legs in Snakes by Modular Evolution of Sonic hedgehog and HOXD Enhancers. Current Biology, 2016; DOI: 10.1016/j.cub.2016.09.020

Sunday, October 23, 2016

Aegean wall lizards switch foraging modes in a human-built environments

Male of Erhard's Wall Lizard (Podarcis erhardii) in the ruins of Ag. Achilleos
 on the small island in Lake Mikri Prespa. Author: Jeroen Speybroeck
The Aegean Wall Lizard, Podarcis erhardii inhabits the Balkan peninsula and the Aegean islands. On the mainland it ranges from Albania, the Republic of Macedonia and southern Bulgaria to the northeastern part of the Peloponnese peninsula in Greece. Donihue (2016) tested for foraging mode switching between populations of the Aegean wall lizard, Podarcis erhardii, inhabiting undisturbed habitat and human-built rock walls on the Greek island of Naxos. He observed foraging behavior among 10 populations and tested lizard morphological and performance predictions at each site. He also investigated the diet of lizards at each site relative to the available invertebrate community.He  found that lizards living on rock walls were significantly more sedentary—sit and wait—than lizards at nonwall sites. He also found that head width increased in females and the ratio of hind limbs to forelimbs in both sexes increased as predicted. Diet also changed, with non-wall lizards consuming a higher proportion of sedentary prey. This study demonstrates microgeographic variability in lizard foraging mode as a result of human land use. In addition, these results demonstrate that foraging mode syndromes can shift intraspecifically with potential cascading effects on local ecological communities. Lacertids are considered a clade of active foraging species and the populations on Naxos from habitats that reflect the pre-human landscape in Greece  were active foragers.

Citation
Donihue CM. 2016. Aegean wall lizards switch foraging modes, diet, and morphology in a human‐built environment. Ecology and Evolution. DOI: 10.1002/ece3.2501

Saturday, October 22, 2016

The snake that ate a lizard, that ate an insect

An interpretive drawing of SMF ME 11332a overlaid on a„ photograph. The lizard, 
Geiseltaliellus maarius (orange), is preserved in the stomach of the snake (white). 
The lizard was swallowed headfirst, and the tail does not appear to have been shed 
during the encounter with the snake. The position of the insect in the abdominal cavity
 of the lizard is indicated in outline (blue).Juliane Eberhart, Anika Vogel. 
A recent paper in  Palaeobiodiversity and Palaeoenvironments Smith and Scanferla (2016) report a fossil snake from the middle Eocene (48 million years ago) Messel Pit, in whose stomach is a lizard, in whose stomach is an insect. This is the second report of a vertebrate fossil containing direct evidence of three trophic levels. The snake is identified as a juvenile of Palaeopython fischeri on the basis of new characters of the skull; the lizard is identified as Geiseltaliellus maarius, a stem-basilisk; and the insect, despite preserved structural colouration, could not be identified. The lizard, G. maariusis is thought to have been an arboreal species, but like its extant relatives may have foraged occasionally on the ground. Another, larger specimen of G. maarius preserves plant remains in the digestive tract, suggesting that omnivory in this species may have been common in larger individuals, as in extant Basiliscus and Polychrus. A general picture of the trophic ecology of P. fischeri is not yet possible, although the presence of a lizard in the stomach of a juvenile individual suggests that this snake could have undergone a dietary shift, as in many extant boines.

Citation

Smith KT, Scanferla A. Fossil snake preserving three trophic levels and evidence for an ontogenetic dietary shift. Palaeobiodiversity and Palaeoenvironments. 2016:1-1.

Thursday, October 20, 2016

A new Andean Shadow Snake and the Diaphorolepidini tribe

Nicéforo María's Shadow Snake, Synophis niceforomariae
The genus Synophis contains a number of enigmatic species, distributed primarily in the Andean highlands of northern South America. Their extreme crypsis and rarity has precluded detailed study of most species. A recent flurry of collection activity resulted in the accession of many new specimens, and the description of 4 new species in 2015, doubling the number of described taxa. However, lingering questions remain regarding the assignment of many new and historical specimens, the morphological limits and geographical ranges of the species, and their phylogenetic relationships. In a new paper Pyron et al. (2016) analyze new and existing morphological and molecular data to produce a new molecular phylogeny and revised morphological descriptions. They also validate the previously unavailable tribe name Diaphorolepidini Jenner, Pyron, Arteaga, Echevarría, & Torres-Carvajal, describe a 9th species, Synophis niceforomariae and offer the new Standard Names in English and Spanish for the group: the Andean Shadow Snakes and Culebras Andinasde la Sombra, respectively. The authors suggest  cryptic and undiscovered diversity undoubtedly remains within the genus. The tribe Diaphorolepidini is based upon the most recent common ancestor of Diaphorolepis wagneri Jan, 1863, Emmochliophis (Synophis) miops (Boulenger, 1898), and Synophis bicolor Peracca, 1896. The new species, Synophis niceforomariae occurs in the Andean highlands of north-central Colombia, Antioquia department, near Medellín, ~1300–1700m, with possible populations south of Medellín, ~900m.


Citation
Pyron RA, Artega A, Echevarria LY, Torres-Carvajal OM. 2016. A revision and key for the tribe Diaphorolepidini (Serpentes: Dipsadidae) and checklist for the genus Synophis. Zootaxa. 4171(2):293-320.

Wednesday, September 7, 2016

Largest snake phylogeny study to date, recovers a new colubrid subfamily

The new subfamily Ahaetuliinae contains Ahaetulla (left) and 
Dryophiops (right). JCM
In a recently published paper in PLoS One Figueroa et al. (2016) provide a species level phylogeny for 1652 snake species and describe a new colubrid subfamily and genus based upon 9,523 base pairs from 10 loci (5 nuclear, 5 mitochondrial), including previously unsequenced genera and species.The increase of taxon sampling resulted in a phylogeny with a new higher-level topology and corroborate many lower-level relationships, strengthened by high nodal support values (> 85%) down to the species level (73.69% of nodes). Although the majority of families and subfamilies were strongly supported as monophyletic with > 88% support values, some families and numerous genera were paraphyletic.  With all rogue taxa and incertae sedis species eliminated, higher-level relationships and support values remained relatively unchanged, except in five problematic clades. Some of the highlights include the following:

Similar to many prior examinations, the authors find relationships within Scolecophidia are unresolved with studies showing either Scolecophidia , Anomalepididae or Leptotyphlopidae + Typhlopoidea as sister to all snakes. They found weak support for the placement of Asiatyphlopinae, Afrotyphlopinae, and Madatyphlopinae within Typhlopidae as in previous studies.

They found Cylindrophiidae is paraphyletic with Anomochilidae and recommend retaining the current classification until more species are sampled.

They recovered for Xenophidiidae + Bolyeridae (SHL = 91). Earlier studies considered these sister to various clades within Henophidia but this study found very strong support (SHL = 100) for them as sister to the Caenophidia (SHL = 100), as shown in other studies. These snakes possess morphological characters, particularly within the palate, bolstering their close relationship with Caenophidia and not to Henophidia. If this placement is retained, then Caenophidia should be redefined to include Xenophidiidae and Bolyeridae, or they should be given their own taxonomic grouping.

The study confirmed previous studies finding that Xenodermatidae is sister to the rest of Colubroidea (SHL = 100) and that relationships within Lamprophiidae and Colubridae remain unresolved, but this study found the placement of Homalopsidae contradicted previous work, and they recovered strong support (SHL = 91) for Homalopsidae + Lamprophiidae, and found Elapidae to be nested within Lamprophiidae. Typically, Lamprophiidae and Elapidae are recovered as distinct clades. Pareatidae is consistently placed as sister to Viperidae, which is sister to Colubridae, Elapidae, Homalopsidae, and Lamprophiidae. 

For Colubridae, the study recovered the following four subclades: i) Sibynophiinae + Natricinae (SHL = 80); ii) Pseudoxenodontinae + Dipsadinae (SHL = 82); iii) Grayiinae + Calamariinae (SHL = 70); and iv) Ahaetuliinae subfam. nov. + Colubrinae (SHL = 95). The nodes between these subclades all received very strong support (SHL > 97). The only consistently recovered clade among these is subclade ii; although other studies did not recover this subclade. Several studies also regularly recovered the subclade Natricinae + (Pseudoxenodontinae + Dipsadinae).  Until now, the basal node of Colubrinae has remained ambiguous. Previous authors suggested that monophyly of Ahaetulla, Chrysopelea, and Dendrelaphis at the base of Colubrinae, may warrant recognition as a distinct subfamily, but support for division of these taxa in their study was low. Due to increased sampling, and the inclusion of Dryophiops, we established strong support for recognizing these taxa as a new subfamily, using the name proposed by Pyron et al, Ahaetuliinae subfam. nov.

Citation
Figueroa A, McKelvy AD, Grismer LL, Bell CD, Lailvaux SP (2016) A Species-Level Phylogeny of Extant Snakes with Description of a New Colubrid Subfamily and Genus. PLoS ONE 11(9): e0161070. doi:10.1371/journal.pone.0161070


Wednesday, August 10, 2016

Colubroid venom composition- an overview

The rear fang of the African Twig snake, Thelotornis capensis.
Snake venoms have been subjected to increasingly sensitive analyses for well over 100 years, but most research has been restricted to front-fanged snakes, which actually represent a relatively small proportion of extant species of advanced snakes. Because rear-fanged snakes are a diverse and distinct radiation of the advanced snakes, understanding venom composition among “colubrids” is critical to understanding the evolution of venom among snakes. In a new paper Junqueira-de-Azevedo and colleagues (2016) review the state of knowledge concerning rear-fanged snake venom composition, emphasizing toxins for which protein or transcript sequences are available. The authors have also added new transcriptome-based data on venoms of three species of rear-fanged snakes. Based on this compilation, it is apparent that several components, including cysteine-rich secretory proteins (CRiSPs), C-type lectins (CTLs), CTLs-like proteins and snake venom metalloproteinases (SVMPs), are broadly distributed among “colubrid” venoms, while others, notably three-finger toxins (3FTxs), appear nearly restricted to the Colubridae (sensu stricto). Some putative new toxins, such as snake venom matrix metalloproteinases, are in fact present in several colubrid venoms, while others are only transcribed, at lower levels. This work provides insights into the evolution of these toxin classes, but because only a small number of species have been explored, generalizations are still rather limited. It is likely that new venom protein families await discovery, particularly among those species with highly specialized diets. The authors conclude that it is now abundantly clear that the venoms produced among the colubrid rear-fanged snakes are homologous with the much better characterized venoms of the front-fanged snakes. As trophic adaptations that facilitate feeding, venoms vary in composition with several important factors, including phylogeny, and so it is to be expected that among the diverse colubrid lineages, novel compounds, and new functional variants of better-known venom proteins, will be encountered. Much progress toward understanding rear-fanged snake venom composition has been made in the last decade, but, as indicated above, we have barely begun to explore the diversity of advanced snakes that comprise the colubrids. Transcriptomic and genomic approaches will greatly facilitate this work, but it must be remembered that functional assays should also accompany analysis of any venom, because the common recurring motif in venom biochemistry is to make the most of a stable molecular scaffold, perhaps best exemplified by the varied pharmacologies of the three-finger toxin superfamily. These small, structurally conservative peptides have very similar crystal structures but affect systems as diverse as neurotransmission, the blood clot cascade, ion channel function, and salamander limb regeneration and courtship. As Dr. Jay Fox once said, in venoms “we find only what we are looking for”, and, to find truly novel toxins that will likely be present in some colubrid venoms, we will have to look beyond the “normal” families of venom proteins.

Junqueira-de-Azevedo, I. L., Campos, P. F., Ching, A. T., & Mackessy, S. P. (2016). Colubrid venom composition: an-omics perspective. Toxins, 8(8), 230.

Viper diversification examined

In a forthcoming paper in MPE Alencar et al (2016) look at the diversification of vipers. The cosmopolitan family contains about 329 venomous species showing a striking heterogeneity in species richness among lineages. While the subfamily Azemiopinae comprises only two species, 70% of all viper species are arranged in the subfamily Crotalinae or the “pit vipers”. The radiation of the pit vipers was marked by the evolution of the heat-sensing pits, which has been suggested to be a key innovation for the successful diversification of the group. Also, only crotalines were able to successfully colonize the New World. The authors present the most complete molecular phylogeny for the family to date that includes sequences from nuclear and mitochondrial genes representing 79% of all living vipers. They also investigated the time of divergence between lineages, using six fossils to calibrate the tree, and explore the hypotheses that suggest crotalines have undergone an explosive radiation. The phylogenetic analyses retrieved high support values for the monophyly of the family Viperidae, subfamilies Viperinae and Crotalinae, and 22 out of 27 genera, as well as well-supported intergeneric relationships throughout the family. The study found strongly supported sister clade to the New World pit vipers that comprises Gloydius, Ovophis, Protobothrops and Trimeresurus gracilis. Time of divergence estimates suggested that vipers started to radiate around the late Paleocene to middle Eocene with subfamilies most likely dating back to the Eocene. The invasion of the New World may have taken place sometime close to the Oligocene/Miocene boundary. Diversification analyses suggested a shift in speciation rates during the radiation of a sub-clade of pit vipers where speciation rates rapidly increased but slowed down toward the present. Thus, the evolution of the loreal pits alone does not seem to explain their explosive speciation rates. The auithor suggest that climatic and geological changes in Asia and the invasion of the New World may have also contributed to the speciation shift found in vipers.

Alencar, L. R., Quental, T. B., Grazziotin, F. G., Alfaro, M. L., Martins, M., Venzon, M., & Zaher, H. (2016). Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution.

An endangered homalopsid snake, Enhydris jagorii

Jagor's Water Snake, Enhydris jagorii. Photo D. R. Karns

Jagor's water snake (Enhydris jagorii) is a freshwater snake endemic to the Chao Phraya-Ta Chin basin of Thailand. Habitat change and destruction are the main threats to this snake, where a large area of the wetland has been rapidly transformed into urban and agricultural areas. Moreover, uncontrolled fishing seriously threatens the what is most likely the last  remaining population of this snake. Pongcharoen et al. (2016) conducted a field study in the Bung Ka Loh wetland from October, 2010 to August, 2014 and collected 108 specimens of this species. Analysis of the stomach contents revealed that it is piscivorous, with cyprinids being the dominant prey. Prey items were usually less than 10% of the snake body mass and multiple prey items were occasionally found. No significant difference in diet was noted between the sexes. In addition, predation on this snake by Cylindrophis ruffus was first recorded in this study. The smallest gravid female collected had a snout-vent length of 34.0 cm. The clutch size and mass ranged from 1 to 28 embryos and 3.1–123.0 g, respectively, and both of these quantities increased significantly with increased female size. Reproduction was possibly seasonal and occurred in the rainy season. A preliminary study of other wetlands in the central plain of Thailand failed to detect the existence of this species. Accordingly, the conservation status of this species should be changed from Data Deficient to Critically Endangered.

Citation
Pongcharoen, C., Voris, H. K., Seelanan, T., Pradatsundarasar, A. O., & Thirakhupt, K. (2016). Diet, female reproduction and conservation of Jagor’s water snake, Enhydris jagorii in Bung Ka Loh wetland, Uttaradit province, Thailand. Agriculture and Natural Resources. Available online 25 June 2016