Sunday, July 26, 2015

A Four-legged fossil snake discovered, and a growing controversy regarding its legal status in Europe

The following has been adapted from a press release and a blog post, with some light editing by me (JCM).
A new fossil, named Tetrapodophis amplectus, claims to be a four-legged, burrowing snake. (A) Counterpart, showing skull and skeleton impression. (B) Main slab, showing skeleton and skull impression. Figure 1 from Martill et al. 2015.  (C) The snake has small ‘hands’ that are approximately 1cm long. Credit: Image courtesy of University of Portsmouth.
The first known fossil of a four-legged snake, and the team -- led by Dr. Dave Martill from the University of Portsmouth -- say that this discovery could help scientists to understand how snakes lost their legs. The research was published in the journal Science.
Dr Martill said: "It is generally accepted that snakes evolved from lizards at some point in the distant past. What scientists don't know yet is when they evolved, why they evolved, and what type of lizard they evolved from. This fossil answers some very important questions, for example it now seems clear to us that snakes evolved from burrowing lizards, not from marine lizards."
The fossil, from Brazil, dates from the Cretaceous period and is 110 million years old, making it the oldest definitive snake. Martill discovered the fossil as part of a routine field trip with students to Museum Solnhofen, Germany, a museum that is well-known for its prestige with regard to fossils.
Dr Martill said: "The fossil was part of a larger exhibition of fossils from the Cretaceous period. It was clear that no-one had appreciated its importance, but when I saw it I knew it was an incredibly significant specimen."
Martill worked with expert German palaeontologist Helmut Tischlinger, who prepared and photographed the specimen, and Nick Longrich from the University of Bath's Milner Centre for Evolution, who studied the evolutionary relationships of the snake.
Dr Longrich, who had previously worked on snake origins, became intrigued when Martill told him the story over a pint at the local pub in Bath.
He said: "A four-legged snake seemed fantastic and as an evolutionary biologist, just too good to be true, it was especially interesting that it was put on display in a museum where anyone could see it."
He said he was initially skeptical, but when Dr Martill showed him Tischlinger's photographs, he knew immediately that it was a fossil snake.
The snake, named Tetrapodophis amplectus by the team, is a juvenile and very small, measuring just 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 two sets of legs, or a pair of hands and a pair of feet.
The front legs are very small, about 1cm long, but have little elbows and wrists and hands that are just 5mm in length. The back legs are slightly longer and the feet are larger than the hands and could have been used to grasp its prey.
Dr Longrich said: "It is a perfect little snake, except it has these little arms and legs, and they have these strange long fingers and toes.
"The hands and feet are very specialized for grasping. So when snakes stopped walking and started slithering, the legs didn't just become useless little vestiges -- they started using them for something else. We're not entirely sure what that would be, but they may have been used for grasping prey, or perhaps mates."
Interestingly, the fossilized snake also has the remains of its last meal in its guts, including some fragments of bone. The prey was probably a salamander, showing that snakes were carnivorous much earlier in evolutionary history than previously believed.
Helmut Tischlinger said: "The preservation of the little snake is absolutely exquisite. The skeleton is fully articulated. Details of the bones are clearly visible and impressions of soft tissues such as scales and the trachea are preserved."
Tetraphodophis has been categorized as a snake, rather than a lizard, by the team due to a number of features:
· The skeleton has a lengthened body, not a long tail.
· 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 displays hints of a single row of belly scales, a sure fire way to differentiate a snake from a lizard.
Tetrapodophis would have lived on the bank of a salt lake, in an arid scrub environment, surrounded by succulent plants. It would probably have lived on a diet of small amphibians and lizards, trying to avoid the dinosaurs and pterosaurs that lived there.
At the time, South America was united with Africa as part of a supercontinent known as Gondwana. The presence of the oldest definitive snake fossil in Gondwana suggests that snakes may originally have evolved on the ancient supercontinent, and only became widespread much more recently.
However there is a controversy brewing around the specimen, and it is not the creationist controversy you might expect.
Discover Magazine’ blog has a piece by Christie Wilcox  titled “Four-Legged Snake Shakes Up Squamate Family Tree – Or Does It?” (posted July 24, 2015)
Ancestral state analyses, use math and science to estimate the biological and ecological traits of the most recent common ancestor of a group of species, suggested that early snakes were nocturnal hunters, preying upon the small vertebrates of their era through stealth, not constriction. Their analysis didn’t find that snakes were burrowers, however — there was no strong support of a fossorial lifestyle, just that the snakes lived on land.
According to Hsiang, morphological data “strongly influenced” the snake tree. “Our study helped to demonstrate how important and essential it is to include fossils when we are trying to understand how and when organisms evolved.” In the paper, the author’s note that the inclusion of fossil data resulted in relationships that would be “unexpected” given current snakes, and that the fossils’ influence was sustained “even when such data are vastly outnumbered by genetic sequence data,” thus including the new fossil in a similar analysis might be even more informative.
“Now that Martill et al.’s paper on Tetrapodophis has been published, the obvious next step is to include it in large-scale, comprehensive analytical studies looking at snake evolutionary history and phylogenies.”
Though there was some excitement when Hsiang and her colleagues published their analysis in May, a paper published a little over a month earlier in PLoS ONE slipped by the press unnoticed. The analysis, led by Tod Reeder from San Diego State University, looked beyond snakes to reconstruct the evolutionary relationships within the squamates, the group of reptiles that contains lizards and snakes. Using the largest dataset to date which, like Hsiang, included both genetic and morphological markers, Reeder and his colleagues affirmed one of the crucial pieces of evidence of a marine snake origin: the close relationship between mosasaurs and snakes.
“The most comprehensive analysis of the lizard evolutionary tree now reinstates these aquatic mosasaurs as the nearest relatives to snakes,” explains Michael Lee, associate professor at the University of Adelaide, who was one of the first scientists to suggest that snakes may have started in the water.
The lizard tree, which found the aquatic mosasaurs (Mosasauria) to be sister to modern snakes (Serpentes).
The lizard evolutionary tree, which places the aquatic mosasaurs (Mosasauria) sister to modern snakes (Serpentes) rather than the group used by Hsiang et al. (Anguimorpha).
Because of this, Reeder et al. calls into question the methods used by Hsiang et al., specifically one of the core assumptions in the paper: the closest relatives of snakes. When constructing evolutionary trees, assumptions have to be made to “root” the tree, or put the relationships into the context with regards to time. Scientists must compare their data to what is called an “outgroup”, which is ideally the closest relative or relatives to the group of interest. Hsiang and her colleagues used a subset of a group of lizards called anguimorphs, which includes land dwelling lizards like varanids that includes the Komodo dragon.
“The Hsiang paper was a terrific analysis of the evolution within snakes, but the fundamental core assumption they made in the paper was that terrestrial lizards were ancestral to snakes,” said Lee. “The direction of evolution was determined by that assumption. But if you assume, as the Reeder paper suggests, that mosasaurs are ancestral to snakes, then some of the inferences by Hsiang might not hold.”
Hsiang admits that there are differences between the phylogenies in her paper and Reeder’s, and that the choice of outgroup may have skewed their results. “There are differences between the Reeder et al. phylogeny and our phylogeny — it would be interesting to conduct an in-depth analysis to try and determine why the differences in phylogeny exist,” she said. While her team’s tree was strongly influenced by morphology, Reeder’s team found that genetics most strongly predicted the results. “In fact, the morphological data are really ambiguous,” co-author John Wiens said in a press release. “Or in some cases, even worse than ambiguous.”
“There’s certainly a possibility that our results would have been different if we had used different outgroups, as phylogenetic and ancestral state reconstruction analyses use the outgroup to determine the direction and polarity of character state evolution,” said Hsiang. However, she doubts the impact would have been large, as other close relatives of mosasaurs are land-lubbers. “Though the inclusion of mosasaurs would likely have increased the probability of an aquatic lifestyle for early snakes somewhat, this would probably have been “balanced out” by the many anguimorph lizards that are not aquatic.”
“Of course, we’d have to actually run the analysis to know for sure.”
Meanwhile, Bruno Simões from the Natural History Museum, London, UK and his colleagues were taking a very different approach to understanding snake evolution. Instead of looking at bones and unrelated genes, they very specifically examined the genes encoding for visual pigments in lizards and snakes. These genes are well-studied, and in other groups like mammals, are correlated with behaviors like burrowing and nocturnal activity.
“Visual pigments, like opsin and rhodopsin, are basically the business front-ends of the visual pathway,” says Simões. “So basically if anything is happening in the visual system, the visual pigments will be the first to be impacted.” Burrowing mammals, for example, have lost some visual pigment genes, as they no longer need them underground. But even more impressively, scientists can connect genetic changes in these pigment genes to ecology and function. “By checking their amino acid composition, you can estimate what kind of wavelengths the animal can see,” says Simões.
When Simões et al. compared the visual pigment genes in snakes to other lizards, they found something exciting: snakes have lost two of the five pigments found in the rest of the squamates. They retain the same three that we have. Simões explained that this means snakes likely went through an “ancestral nocturnal bottleneck,” just like mammals did. “Snakes have this contrasting pattern from lizards that converges with mammals.”
Evolutionary tree for the Rhodopsin 1 gene, the only one left in the most underground snakes.
Interestingly, in fossorial lizards, all five pigments were still around, but in fossorial snakes like the termite-decapitating blindsnakes, only one pigment remained. “The fact that the visual system was not so reduced suggests that the ancestor for all snakes was nocturnal, not fossorial” — a finding which coincides with the ancestral state reconstructions found by Hsiang et al.
As for the question of marine origins, Simões says that he “didn’t find evidence that it was a marine animal.” Marine environments have very different light conditions than terrestrial ones, with a quick loss of red wavelengths with depth, followed by an eventual loss of all light in the deep sea. Marine animals eyes often show a “shift in spectral tuning to a marine environment,” says Simões, which includes a higher sensitivity for blue wavelengths. In sea snakes, for example, the shorter-length opsin 1 becomes blue sensitive instead of UV sensitive. But Simões found no such shift in all snakes.
“I think that it’s a really interesting paper, in that they’ve discovered that snakes have lost a whole bunch of visual genes that are found in other lizards, which does suggest they went through some kind of semi-blind phase in their evolution,” says Lee. But he still would like to see more research before discounting the aquatic hypothesis. “One thing I’d like to see done is what genes are lost in living marine reptiles like sea turtles,” said Lee, to see if there are any opsin genes lost in other marine reptiles like the ones lost in snakes.

A Four-Legged Snake?
Which brings us back to the most recent finding, what Martill and his colleagues claim is a four-legged snake ancestor from Brazil. Though there’s no concrete information about where this fossil originated, the color and texture of the limestone it is encased in suggests it’s from the Crato Formation, a fossil deposit which was laid down some 100 million years ago when the area was a shallow sea.
“The Crato formation is about 20 million years older than the oldest fossil snake,” Martill explained. Thus this ten centimeter-long fossil, which Martill and his colleagues named Tetrapodophis amplectus, may shed light on the earliest snakes.
 “The Martill paper is going to be one of the most controversial papers around for a long time,” said Lee. “I’ve already had about 50 emails from colleagues about it, all expressing really different views.”
“It is a very unusual specimen,” Lee said, “because if it is a snake, it’s a tremendous missing link between lizards and snakes.”
But there are several lineages of lizards with lost or reduced limbs and longer bodies, so the evidence to place it as a snake ancestor must be more than just that. Martill notes that the short length of the tail in relation to the body, structure of the pelvis, impressions of body scales, recurved teeth, high vertebral count and the shape of the vertebrae all make Tetrapodophis a snake. “This thing is much much more of a snake than it is of a lizard,” he concluded. But some scientists don’t buy it. “I think the specimen is important, but I do not know what it is,” University of Alberta paleontologist Michael Caldwell told Ed Yong from National Geographic. But Lee is willing to give Martill the benefit of the doubt. “I’m prepared to provisionally accept that it’s a very unusual small snake,” he said. “But the specimen is so small and the skull is so badly crushed that I think there is going to be a lot of debate until all interested researchers are able to look at it.”
“It does seem to have some pretty intriguing snake features,” Lee admits. “Snake teeth have a very distinct curvature to them… and this animal does seem to have that. So that’s one feature that really makes me think this is probably a snake.” He’s also impressed by the animal’s spine. “It’s got a very large number of vertebrae — 160 backbone elements — which is also a very snake-like feature,” he added. “None of the other features that they list do I find particularly compelling.”
Hsiang, on the other hand, is entirely convinced. “Tetrapodophis does seem to possess many anatomical features that are unique to snakes — the recurved teeth, intramandibular joint, vertebral characters, et cetera,” she said. “So, based on Martill et al.’s report of the anatomy, it seems likely that Tetrapodophis is indeed an early snake.” She’s especially intrigued by what else is visible in the new fossil: its last meal. Martill et al. report that inside the snake’s stomach are a collection of vertebral bones, likely from a small mammal or lizard that it ate just before it died — the same diet that Hsiang et al. predicted with their ancestral state analyses. “The new fossil provides empirical confirmation of some of our results,” she noted. “For instance, the discovery of vertebrate bones in the stomach contents of Tetrapodophis aligns with our inference that the earliest snakes likely ate small vertebrates.”
According to Martill et al., the short tail and reduced limbs are evidence that Tetrapodophis was a burrowing snake. “Although this thing has been found in sediments that were laid down in water,” Martill says, “the shortened limbs and the little scoop-like feet that it’s got on its hind limbs look much more like they’re for burrowing than they are for swimming.”
“Also, they wouldn’t really function for swimming,” Martill said. “This thing is almost certainly using lateral undulatory locomotion to burrow through soft sand and leaf litter.”
“I think that’s fairly weak evidence,” said Lee. “There’s no living burrowing lizard or snake with those type of body proportions,” he added. “We can’t really say what it did at the moment, because there are too many contradictory traits in this animal.”
Lee similarly points to the shape and size of the limbs and feet, but says they provide evidence of an aquatic lifestyle rather than a fossorial one. Species known for their burrowing habits, like moles, have short, squat, strong limb bones, but Tetrapodophis has “long, delicate fingers and toes.” There are also questions about the composition of the bones themselves; bones can vary in the amount of calcium they contain, with more calcium or “more ossified” bones resisting breakage better than less ossified ones. Lee notes that the limbs of Tetrapodophis seem to be “fairly poorly ossified.” “That’s not what you find in burrowers because you want your hands and feet to be as robust as possible to push through the soil.” Reduced ossification of limb bones is, however, a trait shared by other aquatic organisms. Furthermore, in the hind feet, two ankle bones that are fused in most lizards are separate. The only other group of lizards where these bones are apart? The aquatic mosasaurs. Rather than seeing the feet as scoop-like, Lee sees them as “paddle-like.” He also noted that the bones of the fingers and toes are perfectly aligned in parallel with one another. “That leads me to think that they were held together in something, like a flipper or sheath.”
All of that and the fact that the animal was found in what, at the time, was a shallow sea, does give credence to the idea that it could be an aquatic snake. “I wouldn’t come out and say that it’s aquatic, because I don’t think we can say that either,” Lee said, “but I don’t think that we can conclude that it’s burrowing.”
The aquatic idea of snake origins might be the minority view, but there’s enough accumulating evidence now that it needs to be reexamined rather than dismissed out of hand.”
So how die Brazil’s Big Discovery end up in Germany?
Though Tetrapodophis is perhaps the most scientifically-intriguing snake fossil to date, questions about how it arrived in Germany are already beginning to overshadow its scientific importance. Even before the paper officially published, rumors swirled about whether the remarkable specimen was illegally poached from Brazil. When I asked Martill about the specimen’s discovery, he was disturbingly cavalier about the fossil’s origins. “More or less, I discovered it,” he said, “I actually found it in a museum collection.”
“It was one of those serendipitous things,” he continued.  “I actually worked on fossils from this location in Brazil for many many years.” But Martill didn’t find Tetrapodophis on an excursion to the jungle; he found it labeled as an “Unknown Fossil” in the Bürgermeister-Müller Museum in Solnhofen, Germany on a routine class trip for his students. It just so happened that when he took his students to see the museum, on display was an exhibit on Brazilian fossils, which Martill — having written a book about the Crato formation — was excited to see. “All of a sudden, my jaw just dropped to the floor,” he recounts. “This looks like a snake!”
When pressed, he admitted that there was no information about the fossil’s origins — when it was found, who pulled it from the earth, and how or why it made its way across the ocean to a small museum in Germany. He was blunter when he spoke to Herton Escobar (quoted by Herton Escobar for Science). Martill told him that questions about legality are ‘irrelevant to the fossil’s scientific significance’ and said: “Personally I don’t care a damn how the fossil came from Brazil or when.”
As Shaena Montanari explains for Forbes, given the laws in Brazil since 1942, it’s likely that Tetrapodophis found its way to Europe illegally. Brazilian officials have gone as far as to say they’re certain the specimen illegally left the country. Many scientists are expressing their outrage that a prestigious journal like Science would even publish a paper based upon what is likely a black market specimen.
Thus, the specimen is controversial by its very nature but the issue of it being in Germany illegally also raises questions about the fossil trade.

  References
Martill, Tischlinger & Longrich. (2015). A four-legged snake from the Early Cretaceous of Gondwana. Science. doi: 10.1126/science.aaa9208
Hsiang et al. (2015). The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC evolutionary biology, 15(1), 87. doi: 10.1186/s12862-015-0358-5
Reeder et al. (2015) Integrated Analyses Resolve Conflicts over Squamate Reptile Phylogeny and Reveal Unexpected Placements for Fossil Taxa.PLoSONE 10(3): e0118199. doi: 10.1371/journal.pone.0118199
Simões et al. (2015). Visual system evolution and the nature of the ancestral snake. Journal of evolutionary biology 28(7): 1309-1320. doi: 10.1111/jeb.12663
 Read the full interview between Martill and Escobar here

Sunday, July 5, 2015

More on Pseustes poecilonotus as a nest predator

Fragmented tropical forest landscapes are becoming more abundant, and loss of species following fragmentation are often predictable. Larger animals, tend to disappear first from fragments due to the bushmeat trade. However,  another vulnerable group includes understory, insectivorous birds, and ant-following birds. Nest predation is one mechanism that may limit bird populations and has long been suspected as a factor threatening bird populations in temperate  and tropical forest fragments.  A potential influence on nest predation that remains understudied in the tropics is density dependence. Dense territories can increase predators’ ability to find the closely-spaced nests. Yet bird density and nest predation are not always positively correlated, and multiple life-history traits and contexts are relevant.

In a forthcoming paper in Biological Conservation Visco and Sherry (2015) compared nest predation rates, bird density, and predator identities in three habitats of lowland Caribbean Costa Rica: two fragments, a peninsular reserve (La Selva Biological Station), and unfragmented rainforest. Their results suggest an inversely density-dependent nest predation pattern: In fragments, chestnut-backed antbirds reached their highest density and—contrary to predictions—experienced their lowest nest predation rates; La Selva, on the other hand, experienced the lowest density and highest predation rate. Because nest predation decreased with fragmentation, it appears not to explain declines of understory insectivores from forest fragments generally. 

Nest survival models indicated that habitat best-described nest predation likelihood. Video surveillance of nests documented the bird-eating snake (Pseustes poecilonotus) causing 80% of nest loss (37 of 46 nests) and a larger variety of predators in fragments; thus, landscape factors influenced an understory bird’s nest predation. Given the large effect on our focal species, Pseustes likely affects other understory nesters, a topic warranting further study. Tropical reserve conservation plans should consider potential impacts of specialized nest predators on vulnerable understory birds


Citation
Visco, D. M., & Sherry, T. W. (2015 in press). Increased abundance, but reduced nest predation in the chestnut-backed antbird in Costa Rican rainforest fragments: surprising impacts of a pervasive snake species. Biological Conservation.pseutes

Sex reversal triggers rapid transition from genetic to temperature-dependent sex.


Hatchling Bearded Dragon
A climate-induced change of male dragons into females occurring in the wild has been confirmed for the first time, according to University of Canberra research recently published on the cover of international journal Nature.

The researchers, who have long studied Australia's bearded dragon lizards, have been able to show that a reptile's sex determination process can switch rapidly from one determined by chromosomes to one determined by temperature.

Lead author Dr. Clare Holleley, a postdoctoral research fellow at the University of Canberra's Institute for Applied Ecology, explained: "We had previously been able to demonstrate in the lab that when exposed to extreme temperatures, genetically male dragons turned into females."

"Now we have shown that these sex reversed individuals are fertile and that this is a natural occurring phenomenon."

Using field data from 131 adult lizards and controlled breeding experiments, Dr Holleley and colleagues conducted molecular analyses which showed that some warmer lizards had male chromosomes but were actually female.

"By breeding the sex reversed females with normal males, we could establish new breeding lines in which temperature alone determined sex. In doing so, we discovered that these lizards could trigger a rapid transition from a genetically-dependent system to a temperature-dependent system," she said.

"We also found that sex-reversed mothers -- females who are genetic males -- laid more eggs than normal mothers," Dr Holleley said. "So in a way, one could actually argue that dad lizards make better mums."

University of Canberra Distinguished Professor Arthur Georges, senior author of the paper, also highlighted the importance that these discoveries have in the broader context of sex determination evolution.

"The mechanisms that determine sex have a profound impact on the evolution and persistence of all sexually reproducing species," Professor Georges said.

"The more we learn about them, the better-equipped we'll be to predict evolutionary responses to climate change and the impact this can have on biodiversity globally."



Holleley CE, O'Meally D, Sarre SD, Marshall Graves JA, Ezaz T, Matsubara K, Azad B, Zhang X, Georges A.
Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature, 2015; 523 (7558): 79 DOI: 10.1038/nature14574

Thursday, June 18, 2015

A preliminary revision of Asian Pipe Snakes, Cylindrophis

An undescribed pipe snake from Thailand (JCM) and a map 
showing the known taxa.
The Asian Pipe Snake of the Cylindrophiidae contains about ten species. These are burrowing, semi-aquatic snakes that are basal to most other living snakes. Linnaeus (1758) described Anguis maculata from Sri Lanka, Laurenti (1768) described Anguis ruffa described by Laurenti (1768). In 1818 Wagler established the  genus Cylindrophis based upon a type species from Java, Cylindrophis resplendens which was later synonymized with Cylindrophis ruffus by Schlegel (1844). Several additional taxa were described in the 19th and 20 centuries (e.g., Cylindrophis melanotus Wagler 1830, Cylindrophis lineatus Blanford 1881, Cylindrophis isolepis Boulenger 1896, Cylindrophis opisthorhodus Boulenger, 1897, Cylindrophis boulengeri Roux 1911, Cylindrophis aruensis Boulenger 1920, Cylindrophis celebensis Smith 1927, Cylindrophis heinrichi Ahl 1933, Cylindrophis engkariensis Stuebing 1994, Cylindrophis yamdena Smith and Sidik 1998) and one subspecies, Cylindrophis rufus burmanus, Smith 1943). Most taxa are endemic to one island or small island group with the exception of Cylindrophis ruffus which is widespread, in Thailand, Laos, Vietnam, Myanmar, Cambodia, China, Malaysia, Singapore, and several Indonesian islands including Sumatra, Borneo, Java, and Sulawesi.

In a new paper Amarasinghe et al. (2015) examine the systematics of the genus and redefine based only uon specimens from Java Cylindrophis ruffus, they C. burmanus using the type series collected from Myanmar, and designate a lectotype. They identified four groups based on the number of scale rows around the midbody (17, 19, 21, and 23). Among the Cylindrophis examined they discovered two new species: C. jodiae sp. nov. from Vietnam and C. mirzae sp. nov. from Singapore. This paper is a good start on revising the genus but it leaves many undescribed species in places like Sumatra. Borneo, and most of the Indochinese peninsula.



Citation
Amarasinghe AAT, Campbell PD, Hallermann J, Sidik I, Supriatna J, Ineich I. 2015. Two new species of the genus Cylindrophis Wagler, 1828 (Squamata: Cylindrophiidae) from Southeast Asia. Amphibian & Reptile Conservation 9(1): 34–51 (e98).

Friday, June 12, 2015

Feeding system of the Eastern Diamondback Rattlesnake

The Eastern Diamondback Rattlesnake, Crotalus adamanteus, is the largest rattlesnake species and has an exclusively endothermic diet. Although native to seven states in the southeastern Coastal Plain, the species has been extirpated from Louisiana, is listed as endangered in North Carolina, and is currently under consideration for listing as threatened under the Endangered Species Act.

The question of how all of the parts of an organism work together with environmental factors, even when they are changing during an individual’s life is fascinating.  In venomous snakes, ontogenetic changes in diet and intraspecific variation in venoms have been documented. However, the timing of such changes in a life history context and a comparison of the extent of ontogenetic and geographical variation in natural populations have not been investigated.

In an early on-line version of a new paper by Margres et al. (2015), the authors examine the feeding system of the Eastern Diamondback Rattlesnake. They combine venom, morphology (head shape and fang length) and ontogeny over the various environments and geography the snake inhabits. Using a genotype-phenotype map approach, protein expression data, and morphological data they found: ontogenetic effects explained more of the variation in toxin expression variation than geographic effects; both juveniles and adults vary geographically; variation in toxin expression was a result of directional selection; and different venom phenotypes co-varied with morphological traits also are associated with feeding in temporal (ontogenetic) and geographic (functional) contexts.

Venom is ultimately responsible for knocking down prey, and a suite of morphological traits such as gape and fang length should be equally important to the feeding ecology of venomous species. Phenotypic integration is the dependent relationship between different traits that collectively produce a complex phenotype. In venomous snakes, phenotypic integration includes characters as diverse as venom, head shape, and fang length. The optimal depth of venom injection (i.e., fang length) may depend on venom composition which, along with the head shape, may vary with prey size. Morphological differences are associated with variation in venom composition, and phenotypic integration of the complete feeding system, have not been investigated at any level.


This appears to be the first demonstration of phenotypic integration between multiple morphological characters and a biochemical phenotype across populations and age classes. The authors identified copy number variation as the mechanism driving the differences in the venom phenotypes associated with these morphological differences. They also found parallel mitochondrial, venom, and morphological divergence between northern and southern clades suggests that each clade may warrant classification as a separate evolutionarily significant unit.


Sampling sites for Crotalus adamanteus. The authors collected venom and blood samples from 123 C. adamanteus from seven putative populations; 127 preserved C. adamanteus specimens were used for morphological analyses. Phylogenetic analyses identified two distinct clades, one north of the Suwannee River and one south of the Suwannee River, with dating estimates placing the split at approximately 1.27 Ma. Abbreviations: AR, Apalachicola River; Ca, Crotalus adamanteus; SMR, Saint Mary's River; SR, Suwannee River.

Citation

Margres MJ, Wray KP, Seavy M, McGivern JJ, Sanader D, Rokyta DR. (2015). Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus). Molecular Ecology.

Tuesday, May 26, 2015

Modeling the first snake

A reconstruction of the ancestral crown-group snake, 
Artwork by Julius Csotonyi.
The original snake ancestor was a nocturnal, stealth-hunting predator that had tiny hind limbs with ankles and toes, according to new research. Snakes show incredible diversity, with over 3,400 living species found in a wide range of habitats, such as land, water and in trees. But little is known about where and when they evolved, and how their original ancestor looked and behaved. The original snake ancestor was a nocturnal, stealth-hunting predator that had tiny hind limbs with ankles and toes, according to research published in the open access journal BMC Evolutionary Biology.
The study, led by Yale University, USA, analyzed fossils, genes, and anatomy from 73 snake and lizard species, and suggests that snakes first evolved on land, not in the sea, which contributes to a longstanding debate. They most likely originated in the warm, forested ecosystems of the Southern Hemisphere around 128 million years ago.
Snakes show incredible diversity, with over 3,400 living species found in a wide range of habitats, such as land, water and in trees. But little is known about where and when they evolved, and how their original ancestor looked and behaved.
Lead author Allison Hsiang said: "While snake origins have been debated for a long time, this is the first time these hypotheses have been tested thoroughly using cutting-edge methods. By analyzing the genes, fossils and anatomy of 73 different snake and lizard species, both living and extinct, we've managed to generate the first comprehensive reconstruction of what the ancestral snake was like."
By identifying similarities and differences between species, the team constructed a large family tree and illustrated the major characteristics that have played out throughout snake evolutionary history.
Their results suggest that snakes originated on land, rather than in water, during the middle Early Cretaceous period (around 128.5 million years ago), and most likely came from the ancient supercontinent of Laurasia. This period coincides with the rapid appearance of many species of mammals and birds on Earth.
The ancestral snake likely possessed a pair of tiny hind limbs, and targeted soft-bodied vertebrate and invertebrate prey that were relatively large in size compared to prey targeted by lizards at the time. While the snake was not limited to eating very small animals, it had not yet developed the ability to manipulate prey much larger than itself by using constriction as a form of attack, as seen in modern Boa constrictors.
While many ancestral reptiles were most active during the daytime (diurnal), the ancestral snake is thought to have been nocturnal. Diurnal habits later returned around 50-45 million years ago with the appearance of Colubroidea -- the family of snakes that now make up over 85% of living snake species. As colder night time temperatures may have limited nocturnal activity, the researchers say that the success of Colubroidea may have been facilitated by the return of these diurnal habits.
The results suggest that the success of snakes in occupying a range of habitats over their evolutionary history is partly due to their skills as 'dispersers'. Snakes are estimated to be able to travel ranges up to 110,000 square kilometers, around 4.5 times larger than lizards. They are also able to inhabit environments that traditionally hinder the dispersal of terrestrial animals, having invaded aquatic habitats multiple times in their evolutionary history.

Citation
Hsiang AY, Field DJ, Webster TH, Behlke ADB, Davis MD, Racicot RA, Gauthier JA. 2015. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology, 2015; 15 (1) DOI: 10.1186/s12862-015-0358-5

Tuesday, May 19, 2015

Eating-induced changes of the Burmese python's intestines due to changes in gene expression



 The Burmese python's body undergoes massive reconstruction followed by complete deconstruction every time it eats. Within three days of eating, its organs expand up to double in size and its metabolism and digestive processes increase 10- to 44-fold. Ten days after eating, the snake's meal is digested and these changes have reversed, allowing the body to shrink and return back to its pre-meal state. In a new study published in Physiological Genomics, a team of U.S. researchers tracked in detail how this extreme makeover is controlled by changes in gene expression.

The Burmese python's extreme physiology is fascinating to study because it gives unique insight into how vertebrates control organ growth and function, the researchers wrote. Although the Burmese python's body shape is distinct from other vertebrates, including humans, its organs operate the same. This means findings from snakes can be applied to understanding the human body and potentially developing new therapies for human diseases, the researchers said.

In this study, the research team focused on the small intestine, which doubles in mass and nutrient-absorption rate during digestion. The researchers found that the expression of at least 2,000 genes changed after the snake ate. Surprisingly, most of the changes occurred soon after eating -- within six hours. Genes that changed included those involved with the intestine's structure and nutrient absorption, cell division and cell death. The patterns of gene expression matched and often preceded physiological changes in the intestine, the researchers wrote. The gene expression patterns, like the structural changes, then returned to pre-eating state within 10 days after eating, "indicating a tight association between differential gene expression and the rapid and cyclic physiological remodeling of the intestine," the researchers said.

According to the researchers, this is the first study to link the extreme and rapid eating-induced changes of the Burmese python's intestines directly to changes in gene expression, and also the first to show how quickly gene expression changed. The study also found that some of the morphing genes in the python's intestine, notably those in a signaling pathway called WNT, were genes that were involved in intestinal and other cancers. This suggests that "the python intestine may represent a valuable model for studying the interactions of metabolism with the regulation of cell division/death and WNT signaling relevant to cancer," the researchers said.

Citation
Andrew AL, Card DC, Ruggiero RP, Schield DR, Adams RH, Pollock DD, Secor SM, Castoe TA. (2015) Rapid changes in gene expression direct rapid shifts in intestinal form and function in the Burmese python after feeding. Physiological Genomics, 47 (5): 147 DOI: 10.1152/physiolgenomics.00131.2014


Saturday, May 16, 2015

tail length in snakes associated with gravity


An arboreal eyelash viper (Bothriechis schlegelii)
 resting on a branch in Costa Rica. Photograph by 
Coleman M. Sheehy III. 
Gravity is a pervasive force that can severely affect blood circulation in terrestrial animals, and these effects can be particularly pronounced in tall or long organisms such as giraffes and snakes. Upright postures create vertical gradients of gravitational pressures within circulatory vessels that increase with depth. In terrestrial animals, this pressure potentially induces blood pooling and edema in the lower-most tissues and decreases blood volume reaching the head and vital organs.

Since their evolutionary origins about 100 million years ago, snakes have diversified into a wide variety of aquatic, burrowing, terrestrial, and arboreal habitats where they experience various levels of gravitational stress on blood circulation. At the extremes, these stresses range from low to none in fully aquatic species living in essentially “weightless” environments, to relatively high in climbing species, especially arboreal forms specialized for climbing trees. As a result, arboreal snakes exhibit many adaptations for countering the effects of gravity on blood circulation, including relatively tight tissue compartments in the tail. However, patterns of tail length in relation to arboreal habitats and gravity have not been previously studied.

We obtained length data for 226 snake species representing almost all snake families to test the hypothesis that arboreal snakes have longer tails than do non-climbing species. We found that average tail length increased and average body length decreased with increasing use of arboreal habitats and that arboreal snake species had average tail lengths 3–4 times longer than those of non-climbing species. Snakes with longer tails have a higher percentage of elongate blood vessels contained within the relatively tight skin of the tail, which counters blood pooling experienced during climbing. Total body length appears to be constrained in arboreal species, and total body length in adult female arboreal snakes appears to be an evolutionary tradeoff that favors longer tail lengths over maximum production of offspring as arboreal habitat-use increases. Our findings provide evidence that long tails of arboreal snakes function, at least in part, as an adaptation to counter cardiovascular stresses on blood circulation imposed by gravity.


Citation

Sheehy, C. M., Albert, J. S., & Lillywhite, H. B. (2015). The evolution of tail length in snakes associated with different gravitational environments. Functional Ecology. Early On-line.

Friday, May 1, 2015

Geckos evolved daytime activity multiple times

A diurnal Phelsuma and a nocturnal Cyrtodactylus
Geckos are the only clade of lizards that are mostly nocturnal; 72% of the 1552 described species are active at night. Geckos possess numerous adaptations to low light and low temperatures, suggesting nocturnal activity evolved early in their evolution. These adaptations include the evolution of vocalization and acoustic communication, olfactory specialization, enhanced capability for sustained locomotion at low temperatures, shifts in diet and foraging mode, and the absence of the parietal foramen and pineal eye. Geckos have acute vision and many adaptations for seeing in low light including: large eyes, pupils capable of an extreme degree of constriction and dilation, retinas without foveae, short visual focal length, multifocal color vision, and rod-like photoreceptor cells in the retina that lack oil droplets. However, not all gecko species are nocturnal; more than 430 are diurnal. Many of these diurnal lineages have their own adaptations to living in warm, photopic environments including round pupils, UV-filtering crystallin lens proteins, smaller eyes, partial to complete foveae, cone-like photoreceptor cells in the retina and a return to higher energetic costs of locomotion. Geckos are thought to be ancestrally nocturnal and diurnality evolved multiple times. However, this hypothesis has never been tested in a phylogenetic framework.

Now, in a new paper Gamble et al. (2015) performed comparative analyses using a newly generated gecko phylogeny and examined the evolution of temporal activity patterns to: test the hypothesis of an early origin of nocturnality in geckos; verify repeated subsequent transitions to diurnality; and determine whether the evolution of temporal activity patterns has influenced diversification rates. The results provide the first phylogenetic analysis of temporal activity patterns in geckos and confirm an ancient origin of nocturnality at the root of the gecko tree. Gamble et al. identify multiple transitions to diurnality at a variety of evolutionary time scales and transitions back to nocturnality occur in several predominantly diurnal clades.

The authors found several transitions occurred deep in the phylogeny, including ancestors to the Pygopodidae, the New World sphaerodactyl geckos and the Phelsuma plus Lygodactylus clade. More recent transitions occurred in Rhoptropus, within New Zealand and New Caledonian diplodactylids (Naultinus and Eurydactylodes), and within Gymnodactylus, Ptyodactylus and Mediodactylus. Both Asian Cnemaspis clades seem to include multiple transitions, although additional taxonomic sampling is needed to confirm this. They also identified several well-supported eversions to nocturnality within otherwise diurnal clades, including Sphaerodactylus, Gonatodes, Phelsuma and the Pygopodidae. Their results indicate frequent shifts in temporal activity patterns in geckos at a variety of evolutionary timescales. Determining what factors initiate shifts in individual clades was beyond the scope of the paper, but they suggest three possible causes: climate, predators and competition.

Some shifts in activity pattern may be related to thermoregulation and evading extreme temperatures and desiccation. For example, geckos in the genus Sphaerodactylus appear to overheat easily and several species that inhabit hot, xeric habitats are nocturnal, including: S. leucaster, S. thompsoni and S. ladae in southern Hispaniola; S. roosevelti in south-west Puerto Rico; and S. inaguae from the Bahamas. Similarly, some gecko species living at high altitudes, such as Mediodactylus amictopholis, are thought to have shifted to diurnal activity to facilitate thermoregulation in colder climates. However, there are numerous counter inhabiting extreme environments. Pristurus and Rhoptropus, for instance, are diurnal genera that can be active at extremely high temperatures in arid environments while Homonota darwnii and Alsophylax pipiens live in cold climates at extreme latitudes and remain nocturnal. Furthermore, nocturnal geckos seem quite capable of regulating body temperature while hidden in retreats during the day and thus switching to diurnality solely for thermoregulatory purposes may be uncommon overall.

Predation could also instigate changes in temporal activity patterns in geckos and such shifts are well documented in other vertebrate species. Most predator-induced niche shifts in geckos involve the alteration of the spatial niche. However, the hypothesis that geckos may transition to a more conspicuous, diurnal lifestyle in environments where predators are less abundant or absent, such as on islands. Lack of predators is thought to be responsible for dramatic changes in phenotype and behavior in many island species, such as the evolution of flightlessness in birds. Thus, it is reasonable that similar selective pressures could alter temporal activity in geckos.

Shifts in temporal activity patterns may also be related to competition avoidance and the exploitation of underutilized resources. Temporal resource partitioning helps competitors coexist by avoiding direct confrontation or reducing resource overlap. For example, the early shift to nocturnality in ancient geckos has been attributed to avoiding competition with diurnal lizards and exploiting the relatively open nocturnal niche. The lack of competition with other diurnal lizards, mostly iguanians, is frequently cited as promoting transitions back to diurnality in geckos. Indeed, many diurnal geckos occur in regions with a paucity of iguanian species. The success of Phelsuma and Lygodactylus in Madagascar has been attributed to the lack of arboreal iguanians, with the exception of the extremely specialized chameleons.

The scenario presented here will be useful in reinterpreting existing hypotheses of how geckos have adapted to varying thermal and light environments. These results can also inform future research of gecko ecology, physiology, morphology and vision as it relates to changes in temporal activity patterns.

Citation

Gamble T, Greenbaum E, Jackman TR, Bauer AM (2015), Into the light: diurnality has evolved multiple times in geckos. Biological Journal of the Linnean Society. doi: 10.1111/bij.12536

Wednesday, April 29, 2015

Tracking Python bivittatus in Everglades National Park

The largest and longest Burmese Python tracking study of its kind -- here or in its native range -- is providing researchers and resource managers new information that may help target control efforts of this invasive snake, according to a new study led by the U.S. Geological Survey.

Among the findings, scientists have identified the size of a Burmese python's home range and discovered they share some "common areas" that multiple snakes use.

"These high-use areas may be optimal locations for control efforts and further studies on the snakes' potential impacts on native wildlife," said Kristen Hart, a USGS research ecologist and lead author of the study. "Understanding habitat-use patterns of invasive species can aid resource managers in designing appropriately timed and scaled management strategies to help control their spread."
Using radio and GPS tags to track 19 wild-caught pythons, researchers were able to learn how the Burmese python moved within its home range. The 5,119 days of tracking data led researchers to conclude that python home ranges are an average of 22 square kilometers, or roughly an area 3 miles wide-by-3 miles long, all currently within the park.

The study found pythons were concentrated in slough and coastal habitats, with tree islands being the principal feature of common-use areas, even in areas where they were not the predominant habitat type. The longest movements of individual pythons occurred most often during dry conditions, but took place during "wet" and "dry" seasons.

Burmese pythons are long-lived, large-bodied constricting snakes native to Southeast Asia. Highly adaptable, these ambush predators can reach lengths greater than 19 feet and produce large clutches of eggs that can range from eight to 107 eggs. Burmese pythons were first observed in South Florida's Everglades National Park in 1979. Since then, they have spread throughout the park. Although recent research indicates the snakes may be having a significant effect on some populations of mid-sized mammals, it has also shown there is little risk to people who visit Everglades National Park.

Invasive species compete with native wildlife for food, and they threaten native biodiversity across the globe. With nearly 50 percent of the imperiled species in the US being threatened by exotic species, a major concern for land managers is the growing number of exotics that are successfully invading and establishing viable populations.

Florida is home to more exotic animals than any other state. Snakes in particular have been shown to pose a high risk of becoming invasive species. The establishment of Burmese pythons in South Florida poses a significant threat to both the sensitive Everglades ecosystem and native species of conservation concern. For example, in the park, wood storks, Florida panthers and Cape Sable seaside sparrows are all species of conservation concern that have home ranges near the common-use areas of the radio-tracked pythons.

Citation
Kristen M Hart, Michael S Cherkiss, Brian J Smith, Frank J Mazzotti, Ikuko Fujisaki, Ray W Snow, Michael E Dorcas. 2015. Home range, habitat use, and movement patterns of non-native Burmese pythons in Everglades National Park, Florida, USA. Animal Biotelemetry, 3 (1) DOI: 10.1186/s40317-015-0022-2


Monday, April 27, 2015

The endemic freshwater snake Parahelicops boonsongi moved to a new genus

Isanophis boonsongi new comb., preserved 
holotype (FMNH 135328). From top to 
bottom: Dorsal view - Ventral view - 
Lateral view of the head and neck, left side. 
Photographs by Patrick David.
There is little doubt that Southeast Asia harbors the most diverse assemblage of living snake species. And, a number of species from the Indochinese region, including Thailand, are still poorly known only, in some cases known only from their holotype or type series, or at best a handful of specimens. Natricid snakes are particularly diverse in Southeast Asia and three genera contain species that seem to be restricted to very small ranges, they are all aquatic and despite being described in the mid-20th century have remained enigmatic.
Angel’s stream snake, Paratapinophis praemaxillaris described by Angel in 1929, has been known from two syntypes from northern Laos, and six other specimens from China and Thailand. Two other natricine species, Pararhabdophis chapaensis and Parahelicops annamensis both described by Bourret in 1934, were previously known from their respective holotypes. However, Stuart (2006) described a second specimen of P. annamensis, from Laos in 2006. Recently, intensive fieldwork in northern Vietnam and Laos, recovered about 10 specimens of Parahelicops annamensis and Pararhabdophis chapaensis each. Another rare species, Parahelicops boonsongi described by Taylor and Elbel in 1958 was described on the basis of a single specimen from Loei Province in northeastern Thailand. Subsequently, two additional specimens, also from Loei Province were found by Cox in 1995.

Taylor and Elbel placed their new species to the genus Parahelicops because of morphological similarities with P. annamensis, such as the single prefrontal. However, the generic status of Parahelicops has been controversial since its description. It was established by Bourret for a new species, Parahelicops annamensis, on the basis of a single specimen with the following characters: 25 subequal maxillary teeth, the last two enlarged; head quite distinct from the neck; eye small with a round pupil; nostrils directed upwards; two internasals, a single prefrontal; elongated body, slightly laterally compressed; dorsal scales keeled, without apical pits, in 15 rows; tail long; subcaudals paired; hypapophyses developed throughout the vertebral column. Bourret (1934b) also noted its similarity to Opisthotropis but differed in dentition, having its head distinct from the neck, and its elongated body.

Parahelicops boonsongi was described by Taylor and Elbel in 1958 and is known from only three specimens from Thailand. It has been placed either in the genus Parahelicops Bourret, 1934, along with Parahelicops annamensis, as well as the genus Opisthotropis Günther, 1872. In a new paper David et al. (2015) compared its morphological characters with those of P. annamensis and with three other relevant genera, Opisthotropis, Pararhabdophis Bourret, 1934, and Paratapinophis Angel, 1929. Parahelicops boonsongi is phenotypically distinct from Parahelicops annamensis, Opisthotropis, and all other natricine genera. The authors erect a new genus, Isanophis gen. nov., to accommodate Parahelicops boonsongi. How these snakes are related to each other and other natricids remains to be determined.

Citation

David, P., Pauwels, O. S., Nguyen, T. Q., & Vogel, G. (2015). On the taxonomic status of the Thai endemic freshwater snake Parahelicops boonsongi, with the erection of a new genus (Squamata: Natricidae). Zootaxa, 3948(2), 203-217.

Friday, April 17, 2015

The sea snake assemblage in the Muar estuary

Enhydrina schistosa. Photo credit: Aaron Lobo
The first major survey of marine snakes were published by Malcolm Smith and covered the coastal areas of the Gulf of Thailand and the Malay Peninsula between 1915 and 1918 and yielded a collection of 548 sea snakes representing 17 species. These snakes were obtained as by-catch from local coastal fisherman using a variety of fishing techniques. In the late 1930’s and early 1940’s Bergman reported on another large collection of marine snakes from coastal areas near Sourabaya (Surabaya, Java). The collections were made by local fisherman between 1936 and 1942, and consisted of 984 specimens representing six species (3 or more additional species were “disregarded” due to rarity). This collection may represent the first major collection of marine snakes in which all specimens from a single coastal area were caught, retained and identified, thus providing both the species richness and some data on relative abundance.

After World War II the use of mechanized diesel-powered bottom trawlers expanded in Southeast Asia and as the demersal fish harvest increased, so must have the marine snake by-catch. This technology allowed for numerous sea snake surveys that covered very large geographic areas (80,000 to more than 120,000 km2) such as Tonking Bay, the South China Sea, the Sahul Shelf , the Gulf of Carpentaria and northern coast of Australia, the Gulf of Thailand, and coastal areas of Borneo. Although many of these surveys resulted in both a species count and the relative abundance of each species, they lacked value at the level of ecological communities because the areas sampled were vast and often ill defined.  

Now, Voris (2015) reports on an extensive collection of marine snakes obtained from a few stationary stake nets in one locally defined area of about two square kilometers. Each captured snake was identified to species and tallied over a period of nine months to allow for overall estimates of species diversity as well as comparisons of diversity between collections from different stake nets within the area, and between collections made during different tidal cycles. This survey of marine snakes in the mouth of the Muar River had two goals. First, it aimed to determine the overall marine snake diversity in the river mouth. Second, it sought to determine if there might be differences in species diversity on a small spatial scale.

He found the marine snakes that inhabit the mouth of the Muar River have adapted to a very dynamic tidal environment that is relatively small in area and spatially restricted by shorelines on two sides. In addition to the hourly changes in salinity, turbidity, speed of the current and direction of flow, the river also varies in depth. Extensive sampling over many months at Muar revealed an assemblage of marine snakes that included one very common species, three common species, four rare species, and three very rare species that likely represent waifs. These collections strongly support the view that the numerical marine snake species richness for the mouth of the Muar River is eight species.

The 968 adult marine snakes collected at the stake nets at Muar belonged to 11 species in three snake families: Acrochordidae (Acrochordus granulatus), Homalopsidae (Cerberus schneiderii), and Elapidae (Hydrophiini, true sea snakes). This assemblage was strongly dominated by the beaked sea snake, Enhydrina schistosa, with, E. schistosa and three species of Hydrophis (H. melanosoma, H. brookii, and H. torquatus) make up 98% of the snakes.

Although the Muar River sample represents an assemblage from only one river mouth, the eight species observed at Muar falls in the middle of the range of 5 to 12 species recorded in other surveys. Yet, when it comes to relative abundance the strong dominance of E. schistosa in the Muar River mouth community makes the Muar assemblage the least diverse of all comparable surveys. The comparisons highlight the unique nature of the marine snake survey at the mouth of the Muar River, the only discreet estuarial location in the world that has been surveyed for relative abundances of marine snakes.


Citation

Voris, H. K. (2015). Marine Snake Diversity in the Mouth of the Muar River, Malaysia. Tropical Natural History 15:1-20.