Wednesday, December 14, 2016

The number of species of birds and what it says about the number of species of reptiles

This blog usually focuses on non-avian reptiles. However, the research reported here on birds has great implications for how we think about the number of species of reptiles. Birds are the most studied group of vertebrates, reptiles are much less studied. Thus if it is possible to double the number of bird species, the number of reptile species is much, much greater than any of the current estimates.

According the the Reptile Database between February 2008 and August 2016, the number of reptiles increased from 8734 to 10,450, in increase of 1716 species or 19.6%.  Just considering the years between 2010 and 2016 there have been 972 new species of reptiles described. While during that same period (2010 to 2016) only 51 species of birds were described. Thus it would seem that the number of species of reptiles particularly squamates (lizards and snakes) is dramatically higher than my estimate made in my 2011 post.

In time of climate change, habitat destruction, pollution, and other forms of environmental degradation are occurring more rapidly than in previous history - it is entirely possible that many species are becoming extinct before they have been described.
The above map was published in 2012 by Saving Species.The variety of life on Earth is not spread evenly, but is concentrated in very special places. Above the world map is color coded for density of vertebrate species. Colors indicate the highest concentrations of the number of animal species across the world's land masses. Deep reds and yellows cover much of the tropics, indicating a huge number of species. The world’s high latitudes and its deserts are blue, indicating relatively low vertebrate diversity. 
New research led by the American Museum of Natural History suggests that there are about 18,000 bird species in the world -- nearly twice as many as previously thought. The work focuses on "hidden" avian diversity -- birds that look similar to one another, or were thought to interbreed, but are actually different species. Recently published in the journal PLOS ONE, the study has serious implications for conservation practices.

"We are proposing a major change to how we count diversity," said Joel Cracraft, an author of the study and a curator in the American Museum of Natural History's Department of Ornithology. "This new number says that we haven't been counting and conserving species in the ways we want."

Birds are traditionally thought of as a well-studied group, with more than 95 percent of their global species diversity estimated to have been described. Most checklists used by bird watchers as well as by scientists say that there are roughly between 9,000 and 10,000 species of birds. But those numbers are based on what's known as the "biological species concept," which defines species in terms of what animals can breed together.

"It's really an outdated point of view, and it's a concept that is hardly used in taxonomy outside of birds," said lead author George Barrowclough, an associate curator in the Museum's Department of Ornithology.

For the new work, Cracraft, Barrowclough, and their colleagues at the University of Nebraska, Lincoln, and the University of Washington examined a random sample of 200 bird species through the lens of morphology -- the study of the physical characteristics like plumage pattern and color, which can be used to highlight birds with separate evolutionary histories. This method turned up, on average, nearly two different species for each of the 200 birds studied. This suggests that bird biodiversity is severely underestimated, and is likely closer to 18,000 species worldwide.

The researchers also surveyed existing genetic studies of birds, which revealed that there could be upwards of 20,000 species. But because the birds in this body of work were not selected randomly -- and, in fact, many were likely chosen for study because they were already thought to have interesting genetic variation -- this could be an overestimate. The authors argue that future taxonomy efforts in ornithology should be based on both methods.

"It was not our intent to propose new names for each of the more than 600 new species we identified in the research sample," Cracraft said. "However, our study provides a glimpse of what a future taxonomy should encompass."

Increasing the number of species has implications for preserving biodiversity and other conservation efforts.

"We have decided societally that the target for conservation is the species," said Robert Zink, a co-author of the study and a biologist at the University of Nebraska, Lincoln. "So it follows then that we really need to be clear about what a species is, how many there are, and where they're found."

Barrowclough GF, Cracraft J, Klicka J, Zink RM. 2016 How Many Kinds of Birds Are There and Why Does It Matter? PLOS ONE, 2016; 11 (11): e0166307 DOI: 10.1371/journal.pone.0166307

Saturday, December 10, 2016

Two critically endangered sea snakes Aipysurus foliosquama and Aipysurus apraefrontalis

This is a photograph of the rare
short nosed sea snake discovered
on Ningaloo reef, Western Australia.
Photo credit: Grant Griffin, W.A.
Dept. Parks and Wildlife
Scientists from James Cook University have discovered two critically endangered species of sea snakes, previously thought to be extinct, off the coast of Western Australia.

It's the first time the snakes have been spotted alive and healthy since disappearing from their only known habitat on Ashmore Reef in the Timor Sea more than fifteen years ago.

"This discovery is really exciting, we get another chance to protect these two endemic Western Australian sea snake species," says study lead author Blanche D'Anastasi from the ARC Centre of Excellence for Coral Reef Studies at JCU.

"But in order to succeed in protecting them, we will need to monitor populations as well as undertake research into understanding their biology and the threats they face."

The discovery of the critically endangered short nose sea snake was confirmed after a Western Australia Parks and Wildlife Officer, Grant Griffin, sent a photo of a pair of snakes taken on Ningaloo Reef to Ms D'Anastasi for identification.

"We were blown away, these potentially extinct snakes were there in plain sight, living on one of Australia's natural icons, Ningaloo Reef," says Ms D'Anastasi.

"What is even more exciting is that they were courting, suggesting that they are members of a breeding population."

The researchers also made another unexpected discovery, uncovering a significant population of the rare leaf scaled sea snake in the lush seagrass beds of Shark Bay.

The discovery was made 1700 kilometres south of the snakes only known habitat on Ashmore Reef.

"We had thought that this species of sea snake was only found on tropical coral reefs. Finding them in seagrass beds at Shark Bay was a real surprise," says Ms D'Anastasi.

Both leaf scaled and short nosed sea snakes are listed as Critically Endangered under Australia's threatened species legislation, which means they have special protection. Despite the good news of the find, sea snake numbers have been declining in several marine parks, and scientists are at a loss to explain why.

"Many of the snakes in this study were collected from prawn trawl by-catch surveys, indicating that these species are vulnerable to trawling," says Dr Vimoksalehi Lukoschek from the Centre of Excellence for Coral Reef Studies.

"But the disappearance of sea snakes from Ashmore Reef, could not be attributed to trawling and remains unexplained.

"Clearly we need to identify the key threats to their survival in order to implement effective conservation strategies if we are going to protect these newly discovered coastal populations," Dr Lukoschek says.

The most common threat to sea snakes is usually thought to be incidental by-catch from trawling, and indeed, both species were sampled in trawl surveys in Shark Bay and Exmouth Gulf, suggesting that this is indeed a threat. However, trawling does not occur at the Timor Sea reefs because the reefs descend sharply into very deep waters. Thus the declines of these species could not be attributed to trawling. Trawling may be impacting coastal populations of these species. Other potential impacts on sea snakes include loss of habitats and/or prey, disease and recruitment failure due to coastal development, mining exploration and extraction, and climate change. However, until we identify the causes of previous extirpations of Aipysurus group species, it will be challenging to implement effective conservation strategies. Thus, in addition to the need for further field surveys to accurately document the true range extents and population  sizes of species (in coastal Western Australia and elsewhere), it also is critically important that targeted research be conducted to further our understanding of the biology and ecology of sea snakes, and address knowledge gaps about the key threatening processes.

B.R. D'Anastasi, L. van Herwerden, J.A. Hobbs, C.A. Simpfendorfer, V. Lukoschek. New range and habitat records for threatened Australian sea snakes raise challenges for conservation. Biological Conservation, 2016; 194: 66 DOI: 10.1016/j.biocon.2015.11.032

The human visual system has evolved specifically to detect snakes

Examples of a Random Image Structure Evolution (RISE) sequence for 
snake pictures. Participants looked at a sequence of 20 pictures with 
interpolation ration starting from 95% to 0% with steps of 5%. RISE
 sequence gradually changes from unorganized to well discernible. 
Photo credit: Nobuyuki Kawai

A Nagoya University research team uses new image processing tool to confirm human visual system has evolved specifically to detect snakes.

Some studies have suggested that the visual systems of humans and other primates are finely tuned to identify dangerous creatures such as snakes and spiders. This is understandable because, among our ancestors, those who were more able to see and avoid these animals would have been more likely to pass on their genes to the next generation. However, it has been difficult to compare the recognition of different animals in an unbiased way because of their different shapes, anatomical features, and levels of camouflage.

In a study reported recently in PLOS ONE, a pair of researchers at Nagoya University obtained strong support for the idea that humans have heightened visual awareness of snakes. The researchers applied an image manipulation tool and revealed that subjects could identify snakes in much more blurry images than they could identify other harmless animals in equivalent images.

The tool, called Random Image Structure Evolution (RISE), was used to create a series of 20 images of snakes, birds, cats, and fish, ranging from completely blurred to completely clear. The pair then asked subjects to views these images in order of increasing clarity until they could identify the animal in the picture.

"Because of the algorithm that it uses, RISE produces images that allow unbiased comparison between the recognition of different animals," first author Nobuyuki Kawai says. "In the images, the animals are 'camouflaged' in a uniform way, representing typical conditions in which animals are encountered in the wild."

The snakes were increasingly well-identified in the sixth to eighth of 20 images, while the subjects often needed to see the less blurred ninth or tenth images to identity the other animals. "This suggests that humans are primed to pick out snakes even in dense undergrowth, in a way that isn't activated for other animals that aren't a threat," co-author Hongshen He explains.

The findings confirm the Snake Detection Theory; namely, that the visual system of humans and primates has specifically evolved in a way that facilitates picking out of dangerous animals. This work augments understanding of the evolutionary pressures placed on our ancestors.

Nobuyuki Kawai, Hongshen He. Breaking Snake Camouflage: Humans Detect Snakes More Accurately than Other Animals under Less Discernible Visual Conditions. PLOS ONE, 2016; 11 (10): e0164342 DOI: 10.1371/journal.pone.0164342

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.

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.

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.


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.

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."
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.  

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.

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."

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.

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.


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.

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.

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