Tuesday, December 17, 2013

Ancestral squamate viviparous?

The ancestor of snakes and lizards likely gave birth to live young, rather than laid eggs, and over time species have switched back and forth in their preferred reproductive mode, according to research published in print in Ecology Letters Dec. 17.

"This is a very unusual and controversial finding, and a major overturn of an accepted school of thought," said Alex Pyron, Robert F. Griggs Assistant Professor of Biology in the Columbian College of Arts and Sciences at the George Washington University. "Before, researchers long assumed that the ancestor of snakes and lizards laid eggs, and that if a species switched to live birth, it never reverted back. We found this wasn't the case."

The findings push researchers' understanding of the evolution of live birth a lot further back in time to 175 million years ago, showing that live birth has a much more ancient past as a strategy than previously believed. The findings are backed by several recent plesiosaur and mosasaur fossil discoveries and the fossil record of a few lizards from the Cretaceous Period, which had embryos in the mother and had live birth.

Dr. Pyron analyzed an evolutionary tree containing all groups of squamates -- the group that comprises lizards and snakes -- which he and a team of researchers published in the journal BMC Evolutionary Biology earlier this year. The tree, which uses DNA sequencing technology to group thousands of lizards and snakes, includes all families and subfamilies and most genus and species groups.

In total, about 115 groups of lizards and snakes, or about 2,000 species, have live birth. The other 8,000 species lay eggs -- at least right now.

Dr. Pyron is working next to analyze all tetrapods -- a group composed of animals with four legs, such as amphibians, reptiles, birds, mammals and turtles -- to see if there are any new surprises about the evolution of their reproductive modes. He also wants to test the genetics at work behind the evolutionary switching of reproductive mode.

R. Alexander Pyron, Frank T. Burbrink. Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecology Letters, 2013; DOI: 10.1111/ele.12168

Zoonotic pathogens in Crotalus viridis, is there potential for spillover?

Can handling rattlesnakes lead to a spillover of a zoonotic
 organisms to humans?

In his 2012 book Spillover, David Quammen examines zoonotic diseases, pathogens that jump from other animals to humans. The list of diseases that impact humans and have reservoirs in other species is lengthy and sobering. HIV, malaria, SARS, hantavirius, influenza, etc. Quammen does an excellent job tracing the origin of HIV in human populations to the early 20th century in West Africa and discussing the cut-hunter hypothesis. This idea suggests HIV moved from non-human primates (probably chimpanzees) to humans when hunters were butchering bushmeat (chimpanzzees). And, Quammen notes the evidence for at least 12 spillover events for HIV, that is humans were infected a minimum of 12 different times by HIV. While most of the zoonotic diseases that have impacted humans come from bats, rodents, or birds- reptiles seem to have been overlooked. But people certainly kill and butcher rattlesnakes in large numbers during rattlesnake round-ups, an excellent opportunity for a pathogen to jump from Crotalus to humans. A new article suggests the opportunity for a spillover event may be present during such events.

Rattlesnakes make ideal subjects for a variety of different scientific disciplines. The prairie rattlesnake (Crotalus viridis) in Colorado was selected for investigation of its relationship to colonies of black-tailed prairie dogs (Cynomys ludovicianus) to study spatial ecology. A total of 31 snakes were anesthetized and had radiotransmitters surgically implanted.

When captured the snakes underwent the following procedures: (1) they had bacterial culture taken from their mouths for potential isolation of pathogenic bacteria; (2) similarly, they had cloacal bacterial cultures taken to assess potentially harmful bacteria passed in the feces; and (3) they had blood samples drawn to investigate the presence of any zoonotic agents in the serum of the snakes.

The results of the bacterial studies and their implications are discussed in a new article by Kevin Fitzgerald and colleagues. A low incidence of bacterial wound infection has been reported following snakebite. Nevertheless, the oral cavity of snakes has long been known to house a diverse bacterial flora.Fitzgerald and colleagues study, 10 different bacterial species from the mouths of the rattlesnakes, six of which are capable of being zoonotic pathogens and inducing human disease. More studies are necessary to see why more rattlesnake bites do not become infected despite the presence of such pathogenic bacteria. The results of fecal bacteria isolated revealed 13 bacterial species, 12 of which can cause disease in humans. Of the snakes whose samples were cultured, 26% were positive for the presence of the pathogen Salmonella arizonae, one of the causative agents of reptile-related salmonellosis in humans.

It has long been reported that captive reptiles have a much higher incidence than wild, free-ranging species. This study shows the incidence of Salmonella in a wild, free-ranging population of rattlesnakes. In addition, Stenotrophomonas maltophilia was isolated. This is a bacterium associated with wound and soft tissue infections that can lead to sepsis, endocarditis, meningitis, and peritonitis. In addition, this bacterium has been increasingly implicated as an opportunistic pathogen to humans during pregnancies, hospitalizations, malignancies and chemotherapy, chronic respiratory diseases, and presurgical endotracheal intubation. Furthermore, S. maltophilia has an intense resistance to broad-spectrum antibiotics, the results of this study showed the bacterium was resistant to multiple antibiotics.

The results of this work suggest anyone working with snake feces, dead skin, or their carcasses must follow reasonable hygiene protocols. Rattlesnakes tested for West Nile antibodies had positive results but these were invalidated owing to possible cross-reactivity with other unknown viruses, interference with snake serum proteins, and the fact that the test was not calibrated for rattlesnake serum. Still, the interesting implication remains, should we be regularly testing these animals as sentinels against potentially zoonotic diseases. The results of this study clearly show the value of veterinarians in a multidisciplinary study of this sort and the particular skill set they can offer. Veterinarians must get involved in conservation studies if the biodiversity of the planet is to be preserved.

Fitzgerald, Kevin T, Shipley, Bryon K., Newquist, Kristin L.,,Vera, Rebecca, Aryn A.2012. Additional Observations and Notes on the Natural History of the Prairie Rattlesnake (Crotalus viridis) in Colorado. Topics in Companion Animal Medicine. 28:167-176. http://dx.doi.org/10.1053/j.tcam.2013.09.008.

Quammen, D. 2012. Spillover, Animal Infections and the Next Human Pandemic. WW Norton & Co,

Xantusid phylogeny

Xantusia henshawi
The night lizards of the clade Xantusiidae are small-bodied, cryptic lizards endemic to the New World. The clade is characterized by several features that are of phylogenetic interest. (1) monophyletic status of extant taxa Cricosaura, Lepidophyma, and Xantusia; (2) a species endemic to Cuba (Cricosaura typica) of disputed age; (3) origins of the parthenogenetic species of Lepidophyma; (4) pronounced micro-habitat differences accompanied by distinct morphologies in both Xantusia and Lepidophyma; and (5) placement of Xantusia riversiana, the only vertebrate species endemic to the California Channel Islands, which is highly divergent from its mainland relatives.

Brian Noonan and colleagues examined data from multiple gene regions to investigate the phylogeny of Xantusiidae using the most comprehensive taxonomic sampling available to date. Parsimony and partitioned Bayesian analyses of more than 7 kb of mitochondrial and nuclear sequence data from 11 loci confirm that Xantusiidae is monophyletic, and comprises three well-supported clades: Cricosaura, Xantusia, and Lepidophyma. The Cuban endemic Cricosaura typica is well supported as the sister to all other xantusiids. Estimates of divergence time indicate that Cricosaura diverged from the (Lepidophyma + Xantusia) clade 81 million years ago (Ma), a time frame consistent with the separation of the Antilles from North America. Their results also confirm and extend an earlier study suggesting that parthenogenesis has arisen at least twice within Lepidophyma without hybridization, that rock-crevice ecomorphs evolved numerous times within Xantusia and Lepidophyma, and that the large-bodied Channel Island endemic X. riversiana is a distinct, early lineage that may form the sister group to the small-bodied congeners of the mainland.

Noonan, B. P., Pramuk, J. B., Bezy, R. L., Sinclair, E. A., de Queiroz, K., & Sites Jr, J. W. (2013). Phylogenetic relationships within the lizard clade Xantusiidae: Molecular Phylogenetics & Evolution 69:109-122.

Air flow in lizards and their relatives

The upper image is a colorized CT scan showing different airways in the lung of a monitor lizard. The bottom image shows how air flows in a mostly one-way loop through the lizard’s lung, as measured by sensors implanted as part of a University of Utah study. Note how the air flows through adjacent lateral airways (blue and purple) by moving through perforations in the airways’ walls. Photo credit: Emma Schachner, University of Utah.

Dec. 11, 2013 — Air flows mostly in a one-way loop through the lungs of monitor lizards -- a breathing method shared by birds, alligators and presumably dinosaurs, according to a new University of Utah study.
The findings -- published online Dec. 11 in the journal Nature -- raise the possibility this breathing pattern originated 270 million years ago, about 20 million years earlier than previously believed and 100 million years before the first birds. Why remains a mystery.

"It appears to be much more common and ancient than anyone thought," says C.G. Farmer, the study's senior author and an associate professor of biology at the University of Utah. "It has been thought to be important for enabling birds to support strenuous activity, such as flight. We now know it's not unique to birds. It shows our previous notions about the function of these one-way patterns of airflow are inadequate. They are found in animals besides those with fast metabolisms."

But Farmer cautions that because lizard lungs have a different structure than bird and alligator lungs, it is also possible that one-way airflow evolved independently about 30 million years ago in the ancestors of monitor lizards and about 250 million years ago in the archosaurs, the group that gave rise to alligators, dinosaurs and birds. More lizard species, such as geckos and iguanas, must be studied to learn the answer, she says.
Farmer conducted the study with two University of Utah biologists -- first author and postdoctoral fellow Emma Schachner and doctoral student Robert Cieri -- and with James Butler, a Harvard University physiologist.

The research was funded by the American Association of Anatomists, the American Philosophical Society, the National Science Foundation and private donor Sharon Meyer.

Tidal Versus One-Way Airflow in the Lungs
Humans and most other animals have a "tidal" breathing pattern: Air flows into the lungs' branching, progressively smaller airways or bronchi until dead-ending at small chambers called alveoli, where oxygen enters the blood and carbon dioxide leaves the blood and enters the lungs. Then the air flows back out the same way.

Birds, on the other hand, have some tidal airflow into and out of air sacs, but their breathing is dominated by one-way airflow in the lung itself. The air flows through the lung in one direction, making a loop before exiting the lung.

In 2010, Farmer published a study showing that a mostly one-way or "unidirectional" airflow controlled by aerodynamic valves exists in alligators. That means the breathing pattern likely evolved before 250 million years ago, when crocodilians -- the ancestors of alligators and crocodiles -- split from the archosaur family tree that led to the evolution of flying pterosaurs, dinosaurs and eventually birds.

The new study found a mostly one-way, looping air flow in African savannah monitor lizards, Varanus exanthematicus -- one of roughly 73 species of monitor lizards -- although there was some tidal airflow in regions of the lungs. That means one-way airflow may have arisen not among the early archosaurs about 250 million years ago, but as early as 270 million years ago among cold-blooded diapsids, which were the common, cold-blooded ancestors of the archosaurs and Lepidosauromorpha, a group of reptiles that today includes lizards, snakes and lizard-like creatures known as tuataras.

One-way airflow may help birds to fly without passing out at high altitudes, where oxygen levels are low. Before the new study, Farmer and others had speculated that the one-way airflow may have helped dinosaurs' ancestors dominate the Earth when atmospheric oxygen levels were low after the Permian-Triassic mass extinction -- the worst in Earth's history -- 251 million years ago.

"But if it evolved in a common ancestor 20 million years earlier, this unidirectional flow would have evolved under very high oxygen levels," she says. "And so were are left with a deeper mystery on the evolutionary origin of one-way airflow."

How the Study was Performed
As in her earlier research on alligators, Farmer and colleagues demonstrated predominantly one-way airflow in the lungs of monitor lizards in several ways. They performed CT scans and made 3-D images of lizard lungs to visualize the anatomy of the lungs. They surgically implanted flow meters in the bronchi of five monitor lizards to measure airflow direction.

Using lungs removed from 10 deceased lizards, the researchers measured air flow as they pumped air into and out of the lungs. They also pumped water laden with sunflower pollen particles or plastic microspheres through lizard lungs, and the movement of the pollen and spheres also showed the unidirectional airflow.
Savannah monitor lizards were used in the research because they are relatively large and thus easier to study, weighing about a pound and measuring roughly 15 inches from head to tail tip. Monitor lizards also have some of the highest rates of oxygen consumption, partly because they breathe using not only their trunk muscles and ribs, but also using "gular pumping," which is when the lizards flare out their throat and pump air into their lungs.

Monitor lizards' lungs have more than a dozen chambers or bronchi in each lung. The primary airway runs the length of the lung, with lateral bronchi branching off of it.

The study showed that air enters the lizard's trachea or windpipe, then flows into the two primary airways, which enter the lung. But then, instead of flowing tidally back out the same way, the air instead loops back in a tail-to-head direction moving from one lateral airway to the next through small perforations between them.
The walls containing perforations that allow air to flow from one chamber to the next "are like lace curtains," Farmer says.

There appear to be no mechanical valves or sphincters, so the one-way airflow appears "to arise simply from jetting," or aerodynamic valves created when air flows around bends within the lung airways. That is supported by the fact that one-way airflow was observed even in lungs removed from dead lizards.

A 60-megabyte movie of CT scans of a lizard's airways may be downloaded here: http://www.hightail.com/download/OGhkQndONEg5eFZFQmNUQw

Emma R. Schachner, Robert L. Cieri, James P. Butler & C. G. Farmer. Unidirectional pulmonary airflow patterns in the savannah monitor lizard. Nature, 2013 DOI: 10.1038/nature12871

Wednesday, December 11, 2013

Lampropeltis triangulum now seven species

A new early on-line study examines reports unrecognized diversity in the milksnake (Lampropeltis triangulum) Coalescent species delimitation indicates that L. triangulum is not monophyletic and that there are multiple species of milksnake, which increases the known species diversity in the genus Lampropeltis by 40%. Both genealogical and temporal discordance occurs between gene trees and the species tree, with evidence that mtDNA introgression is a main factor. The highlights of the study include the following.

1) Lampropeltis triangulum: from Ontario, Canada along the Georgian Bay, throughout southern Quebec, and east of Lake Huron, extending throughout southern Maine, south through New England and New York to North Carolina and the extreme northern Alabama and Georgia and west to eastern Minnesota. Subspecies synonymized under L. triangulum would include L. t. syspila and any suspected “intergrades” that occur in Alabama, Indiana, Iowa, Illinois, Kentucky, Missouri, Mississippi, Tennessee, and possibly Arkansas north of the Arkansas River, and some milksnakes that have fallen under the subspecies L. t. amaura in northeastern Louisiana (specifically in La Salle Parish).

2) Lampropeltis gentilis: Found from the Panhandle of northern Texas, western Oklahoma, central and western Kansas, eastern Colorado, and south-central and southwestern Nebraska. The range of L. gentilis also includes the ranges of the following subspecies, which are synonymized with L. gentilis: L. t. amaura (part), found in eastern Texas, southeastern Oklahoma, Louisiana west of the Mississippi River, and southern Arkansas; L. t. celaenops in southeastern Arizona, New Mexico and adjacent eastern Texas; L. t. multistriata, found in northwestern Nebraska, the western half North Dakota, northern Wyoming, and southern Montana; and L. t. taylori found in Utah, northern Arizona, and western Colorado. In addition, L. gentilis includes L. t. annulata from at least central Texas and L. t. syspila from Nebraska, Kansas, and Oklahoma.

3) Lampropeltis elapsoides: southeastern US as far north as Virginia and Kentucky east of the Mississippi River and in eastern Louisiana. Suspected “intergrades” with L. triangulum from eastern Virginia to southern New Jersey are likely L. triangulum and not hybrids.

4) Lampropeltis annulata: Mexican states of Nuevo León, Querétaro, and Tamaulipas. It is likely that this species is also found in Coahuila, eastern San Luis Potosi, and Hidalgo. Subspecies synonymized with L. annulata include L. t. dixoni.

5) Lampropeltis polyzona: Mexican states of Colima, Guerrero, Hidalgo, Jalisco, Puebla, Michoacán, Oaxaca, Sinaloa, Sonora, and Veracruz. It is likely that this species is also found in Guanajuato, Morelos, and Nayarit, and western San Luis Potosí.

6) Lampropeltis abnorma: southern Veracruz and southeastern Guerrero ranging south through Nicaragua, Honduras, and western Costa Rica. This species is possibly in southern Oaxaca, and likely Campeche, Chiapas, Quintana Roo, Tabasco, and Yucatan as well as Belize and El Salvador. . Subspecies synonymized with L. abnorma include L. t. blanchardi, L. t. hondurensis, L. t. oligozona and L. t. stuarti.

7) Lampropeltis micropholis: eastern Costa Rica, throughout Panama, and south to Ecuador. It is likely found in Colombia and possibly Venezuela. Subspecies synonymized with L. micropholis include L. t. gaigeae and L. t. andesiana.

Sara Ruane, Robert W. Bryson, Jr., R. Alexander Pyron, and Frank T. Burbrink (2014) Coalescent Species Delimitation in Milksnakes (genus Lampropeltis) and Impacts on Phylogenetic Comparative Analyses. Systematic Biology early on-line December 10, 2013 doi:10.1093/sysbio/syt099

New molecular study provides insights into boa and python evolution

Henophidian snakes (boas, pythons, and their relatives) are one of the most spectacular groups of reptiles and constitute a vast diversity of morphologies, behaviors, body sizes and ecologies. This group include both the shortest (the black-bellied dwarf boa, Tropidophis nigriventris, about 250 mm in total length) and longest (reticulated python, about 10 m in total length henophidian snakes. These are constricting snakes, and include the 13 m Titanoboa cerrejonensis possibly the longest snake to ever exist. Henophidians are also represented by enigmatic and hyper-diverse families such as the Tropidophiidae (the dwarf boas) and Uropeltidae (the shield-tailed snakes); as well as by the nearly extinct insular Mascarene family Bolyeriidae. Boas (Boidae) and pythons (Pythonidae) represent highly diverse families with almost global tropical and subtropical distributions. Molecular phylogenetic and biogeographic studies of the boas and pythons have yielded important insights into evolutionary processes as well as an understanding of taxonomy, divergence, and diversification is becoming especially relevant given that many boa and python species are of significant conservation concern.

In an early online view of a new study Graham Reynolds and colleagues use both new and previously published sequence data, to produced a species-level phylogeny for 84.5% of boid species and 82.5% of pythonid species, set within a larger phylogeny of henophidian snakes. They obtained new sequence data for three boid, one pythonid, and two tropidophiid taxa which have never previously been included in a molecular study, in addition to generating novel sequences for seven genes across an additional 12 taxa. The authors compiled an 11-gene data set for 127 taxa, consisting of the mitochondrial genes CYTB, 12S, and 16S, and the nuclear genes bdnf, bmp2, c-mos, gpr35, rag1, ntf3, odc, and slc30a1, totaling up to 7561 base pairs per taxon.They analyzed this dataset using both maximum likelihood and Bayesian inference and recovered a well-supported phylogeny.

Significant evidence was found for the  discordance between taxonomy and evolutionary relationships in the genera Tropidophis, Morelia, Liasis, and Leiopython, and they found support for elevating two previously suggested boid species. they suggest a revised taxonomy for the boas (13 genera, 58 species) and pythons (8 genera, 40 species).

Some of the highlights of the study:

The authors continue to recognize Aniliidae for the Neotropical pipe snake. Tropidophiidae contains both Tropidophis (which is polyphyletic and Trachyboa). The Southeast Asian dwarf pipe snakes (Anomochilidae) are the sister to the Old World pipe snakes (Cylindrophiidae). Collectively the Eastern Hemisphere pipe snakes are the sister to the shield-tailed snakes (Uropeltidae). The sunbeam snakes form the family Xenopeltidae and the Mexican python is placed in the family Loxocemidae.Within the Pythonidae, Python is an Afro-Asian genus (regius, curtus, brogersmai, molurus, bivittaus, anchietae, and sebae). The new genus Malayopython  contains timorensis and reticulatus. Morelia  (carinata, bredi, spilota, viridis) is polyphyletic.

The new study recovered the monotypic Central American Loxocemidae (Loxocemus bicolor) as sister to the in-group pythons, while the East Asian Xenopeltidae (X. hainanensis and X. unicolor) form the sister to the clade (Pythonidae, Loxocemidae) in both analyses. Among the pythons, they found the African and southern Asian genus Python to be a monophyletic clade basal to the rest of the pythons. Within this genus there was support for a basal placement of the small-bodied West African P. regius and a derived clade of large bodied species (P. bivittatus and P. molurus) from southern Asia and a derived clade of the small-bodied Southeast Asian blood pythons (P. brongersmai and P. curtus). This suggests an evolution of gigantism separate from other giant members of the Australasian Pythonidae (Malayopython and Morelia). They also generated novel sequence data for the small-bodied Kalaharian P. anchietae. The subgeneric name Simalia Gray 1849 is used for the scrub python clade.

As for the Boidae, the authors found weak support for a sister relationship of the non-boid Calabaria to the Madagascan boids. As this is not well supported and inconsistent with previous studies, which have all found Calabaria to be basal to the rest of the boid radiation they consider Calabaria as the closest extant relative to the Boidae. Among Malagasy species they found strong support for the distinction of Sanzinia and Acrantophis.

They recovered the Central American Ungaliophis and Exiliboa as sister taxa to the North American boids Charina and Lichanura, with support for the distinction of C. bottae and C. umbratica.

With the first published sequence data for the African species Eryx muelleri, they found strong support for the placement of this species as sister to the south Asian E. jayakari. And found evidence for interdigitation of Eryx species between Africa and south Asia suggesting repeated dispersal events. No evidence was found for the continued use of the generic name Gongylophis.

Among western hemisphere boids, support was found for the recognition of B. imperator and recommend the epithet B. imperator.

As in previous studies the South American Eunectes and Epicrates were recovered as sisters with support for the distinction of the five mainland species of Epicrates. And, they found support for the continued use of the genus Chilabothrus for the island boas formerly in the genus Epicrates.

Graham Reynolds, R., M. L. Niemiller, L. J. Revell. (2013) Toward a Tree-of-Life for the boas and pythons: Multilocus species-level phylogeny with unprecedented taxon sampling. Molecular Phylogenetics and  Evolution. http://dx.doi.org/10.1016/j.ympev.2013.11.011

Monday, December 9, 2013

Crocodilians Lure Prey

Dec. 4, 2013 — Turns out the crocodile can be a shrewd hunter himself. A University of Tennessee, Knoxville, researcher has found that some crocodiles use lures to hunt their prey.
A mugger crocodile balances twigs on its nose to tempt birds 
collecting small branches to build nests with, at Madras 
Crocodile Bank, Tamil Nadu in India. Photo Credit: Vladimir Dinets.
Vladimir Dinets, a research assistant professor in the Department of Psychology, is the first to observe two crocodilian species -- muggers and American alligators -- using twigs and sticks to lure birds, particularly during nest-building time.

The research is published in the current edition of Ethology, Ecology and Evolution. Dinets' research is the first report of tool use by any reptiles, and also the first known case of predators timing the use of lures to a seasonal behavior of the prey -- nest-building.
Dinets first observed the behavior in 2007 when he spotted crocodiles lying in shallow water along the edge of a pond in India with small sticks or twigs positioned across their snouts. The behavior potentially fooled nest-building birds wading in the water for sticks into thinking the sticks were floating on the water. The crocodiles remained still for hours and if a bird neared the stick, they would lunge.

To see if the stick-displaying was a form of clever predation, Dinets and his colleagues performed systematic observations of the reptiles for one year at four sites in Louisiana, including two rookery and two nonrookery sites. A rookery is a bird breeding ground. The researchers observed a significant increase in alligators displaying sticks on their snouts from March to May, the time birds were building nests. Specifically, the reptiles in rookeries had sticks on their snouts during and after the nest-building season. At non-rookery sites, the reptiles used lures during the nest-building season.

"This study changes the way crocodiles have historically been viewed," said Dinets. "They are typically seen as lethargic, stupid and boring but now they are known to exhibit flexible multimodal signaling, advanced parental care and highly coordinated group hunting tactics."
The observations could mean the behavior is more widespread within the reptilian group and could also shed light on how crocodiles' extinct relatives -- dinosaurs -- behaved.

"Our research provides a surprising insight into previously unrecognized complexity of extinct reptile behavior," said Dinets. "These discoveries are interesting not just because they show how easy it is to underestimate the intelligence of even relatively familiar animals, but also because crocodilians are a sister taxon of dinosaurs and flying reptiles."
Dinets collaborated with J.C and J.D. Brueggen from the St. Augustine Alligator Farm Zoological Park in St. Augustine, Fla. More of his crocodile research can be found in his book "Dragon Songs."

V. Dinets, J.C. Brueggen & J.D. Brueggen , Ethology Ecology & Evolution (2013): Crocodilians use tools for hunting, Ethology Ecology and Evolution,

Monday, December 2, 2013

Two snake genomes

The Burmese python's ability to ramp up its metabolism and enlarge its organs to swallow and digest prey whole can be traced to unusually rapid evolution and specialized adaptations of its genes and the way they work, an international team of biologists says in a new paper. Lead author Todd Castoe, an assistant professor of biology at The University of Texas at Arlington College of Science, and 38 co-authors from four countries sequenced and analyzed the genome of the Burmese python, or Python molurus bivittatus. Their work is scheduled for publication this week (Dec. 2) by the Proceedings of the National Academy of Sciences along with a companion paper on the sequencing and analysis of the king cobra (Ophiophagus hannah). The papers represent the first complete and annotated snake genomes.

Python bivittatus (top), Ophiophagus hannah (bottom)
Because snakes contain many of the same genes as other vertebrates, studying how these genes have evolved to produce such extreme and unique characteristics in snakes can eventually help explain how these genes function, including how they enable extreme feats of organ remodeling. Such knowledge may eventually be used to treat human diseases.

"One of the fundamental questions of evolutionary biology is how vertebrates with all the same genes display such vastly different characteristics. The Burmese python is a great way to study that because it is so extreme," Castoe, who began working on the python project as a postdoctoral fellow at the University of Colorado School of Medicine in the laboratory of associate professor and paper corresponding author David D. Pollock.

Castoe said: "We'd like to know how the snake uses genes we all have to do things that no other vertebrates can do."

The new python study calls into question previous theories that major obvious physical differences among species are caused primarily by changes in gene expression. Instead, it contends that protein adaptation, gene expression and changes in the structure of the organization of the genome itself are all at work together in determining the unusual characteristics that define snakes, and possibly other vertebrates.

Pollock said the python and king cobra studies represent a significant addition to the field of "comparative systems genomics -- the evolutionary analysis of multiple vertebrate genomes to understand how entire systems of interacting genes can evolve from the molecules on up."

He said: "I believe that such studies are going to be fundamental to our ability to understand what the genes in the human genome do, their functional mechanisms, and how and why they came to be structured the way they are."

The Burmese python's phenotype, or physical characteristics, represents one of the most extreme examples of evolutionary adaptation, the authors said. Like all snakes, its evolutionary origin included reduction in function of one lung and the elongation of its mid-section, skeleton and organs. It also has an extraordinary ability for what researchers call "physiological remodeling."

Physiological remodeling refers to the process by which pythons are able to digest meals much larger than their size, such as chickens or piglets, by ramping up their metabolism and increasing the mass of their heart, liver, small intestine and kidneys 35 percent to 150 percent in only 24 to 48 hours. As the digestion is completed, the organs return to their original size within a matter of days. The authors suggest that understanding how snakes accomplish these tremendous feats could hold vital clues for the development of treatments for many different types of human diseases.

"The Burmese python has an amazing physiology. With its genome in hand, we can now explore the many untapped molecular mechanisms it uses to dramatically increase metabolic rate, to shut down acid production, to improve intestinal function, and to rapidly increase the size of its heart, intestine, pancreas, liver, and kidneys," said Stephen Secor, associate professor of biological sciences at the University of Alabama and a co-author on the paper. 'The benefits of these discoveries transcends to the treatment of metabolic diseases, ulcers, intestinal malabsorption, Crohn's disease, cardiac hypertrophy and the loss of organ performance."

To complete their work, the research team aligned 7,442 genes from the python and cobra with genes sequences available in the Ensembl Genome Browser from other amphibians, reptile, bird and mammals. They used a statistical method called "branch site codon modeling" to look for genes that had been positively selected (or evolutionarily changed due to natural selection) in the python, the cobra, and early in snake evolution in the common ancestor of these two snakes. They found changes in hundreds of genes. They believe the results demonstrate that natural selection-driven changes in many genes that encode proteins contributed substantially to the unique characteristics of snakes.

Analyses showed a remarkable correspondence between the function of the selected genes, and the many functionally unique aspects of snake biology -- such as their unique metabolism, spine and skull shape and cell cycle regulation, Castoe said. Many of the altered genes the team observed also have prominent medical significance. For example, the python genome showed some changes to the gene GAB1, which other research suggests plays a role in breast cancer, melanomas and childhood leukemia.

In addition to changes to individual genes and their expression, researchers also found that the extreme characteristics in snakes could also be linked to duplications or losses in multigene families. Some of those include ancient loss and more recent re-evolution of high resolution vision, and their ability to detect chemical cues from the environment. Researchers also observed that, while most assume that reptile genes and genomes change at a very slow rate, snake genomes evolve at one of the fastest rates of any vertebrate.

Freek J. Vonk, Nicholas R. Casewell, Christiaan V. Henkel, Alysha M. Heimberg, Hans J. Jansen, Ryan J. R. McCleary, Harald M. E. Kerkkamp, Rutger A. Vos, Isabel Guerreiro, Juan J. Calvete, Wolfgang Wüster, Anthony E. Woods, Jessica M. Logan, Robert A. Harrison, Todd A. Castoe, A. P. Jason de Koning, David D. Pollock, Mark Yandell, Diego Calderon, Camila Renjifo, Rachel B. Currier, David Salgado, Davinia Pla, Libia Sanz, Asad S. Hyder, José M. C. Ribeiro, Jan W. Arntzen, Guido E. E. J. M. van den Thillart, Marten Boetzer, Walter Pirovano, Ron P. Dirks, Herman P. Spaink, Denis Duboule, Edwina McGlinn, R. Manjunatha Kini, and Michael K. Richardson. 2013. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. PNAS 2013 ; published ahead of print December 2, 2013, doi:10.1073/pnas.1314702110.

Todd A. Castoe, A. P. Jason de Koning, Kathryn T. Hall, Daren C. Card, Drew R. Schield, Matthew K. Fujita, Robert P. Ruggiero, Jack F. Degner, Juan M. Daza, Wanjun Gu, Jacobo Reyes-Velasco, Kyle J. Shaney, Jill M. Castoe, Samuel E. Fox, Alex W. Poole, Daniel Polanco, Jason Dobry, Michael W. Vandewege, Qing Li, Ryan K. Schott, Aurélie Kapusta, Patrick Minx, Cédric Feschotte, Peter Uetz, David A. Ray, Federico G. Hoffmann, Robert Bogden, Eric N. Smith, Belinda S. W. Chang, Freek J. Vonk, Nicholas R. Casewell, Christiaan V. Henkel, Michael K. Richardson, Stephen P. Mackessy, Anne M. Bronikowsi, Mark Yandell, Wesley C. Warren, Stephen M. Secor, and David D. Pollock. 2013. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. PNAS 2013 ; published ahead of print December 2, 2013, doi:10.1073/pnas.1314475110

Thursday, November 28, 2013

Sub-lethal skin sections in the wrinkled frog effective against snake predation

Frogs and toads are packets of proteins and calories to many predators. In response anurans have evolved a plethora of defenses against their predators, many of these defenses are chemical. Dendrobatid frogs may kill a potential predators with its defensive toxins, but many species of anurans seem to produce toxins that are sub-lethal. Anuran skin secretions may also have other functions, such as antibacterial protection for their skin. But defensive molecules are abundant in a more or less defenseless group of amphibians.
The Japanese striped snake, Elaphe quadrivirgata,, and the prey it usually avoids, Glandirana (Rana) rugosa.
Photo credit: Alpsdake, and Open Cage.
Some molecules produced by frogs alter the predator's behavior. African clawed frogs  induce yawning and gaping movements in the northern water snake Nerodia sipedon as well as two other natural predators, the African aquatic snakes Lycodonomorphus rufulus and L. laevissimus.

In a new study Yoshimura and Kasuya (2013) examine the impact of the molecules produced by the adult wrinkled frog (Glandirana (Rana) rugosa) which has warty skin with a secretion that has a strong and unique odor. The wrinkled frog is rarely found in the natural diet of the Japanese striped snake (Elaphe quadrivirgata), which is considered a general predator of amphibians, mammals, birds, and reptiles. In a previous study, newborn Japanese striped snake with no prey experience ate few wrinkled frogs. When adult Japanese striped snakes  were forced to swallow wrinkled frogs, all the snakes spat out the frogs and opened and closed their mouths in a gaping behavior. The snake did not change its movements or other behaviors and they did not die shortly after contact with the wrinkle frog. These observations suggested that wrinkled frogs are not highly toxic but that they escape from predation by snakes.

Yoshimura and Kasuya (2013) conducted two experiments to examine whether the skin secretion of adult wrinkled frogs is effective for the evasion of predation by snakes. In the first experiment , they compared the proportion of snakes that bit and swallowed wrinkled frogs with the proportion that bit and swallowed the cricket frog, Fejervarya limnocharis, which resembles wrinkled frogs in size and appearance. In the second experiment they coated the natural prey organisms of the snakes with secretions from the wrinkled frog or the cricket frog to examine the effects of the secretions.

They found the wrinkle frog was less frequently bitten or swallowed by snakes. The snakes that bit wrinkled frog spat out the frogs and showed mouth opening (gaping) behavior, while the snakes that bit the cricket frogs did not show gaping behavior. They also compared the responses of the snakes to wrinkled frogs and F. limnocharis secretions. They coated palatable Rana japonica with secretions from wrinkled frogs or cricket frogs. The frogs coated by wrinkled frog's secretion were less frequently bitten or swallowed than those coated by F. limnocharis secretion. The authors concluded that compared to different frog species of similar sizes, the adult wrinkled frog was less frequently preyed upon by, and that its skin secretion was effective in avoiding predation by snakes.

Yoshimura Y, Kasuya E (2013) Odorous and Non-Fatal Skin Secretion of Adult Wrinkled Frog (Rana rugosa) Is Effective in Avoiding Predation by Snakes. PLoS ONE 8(11): e81280. doi:10.1371/journal.pone.0081280

Wednesday, November 27, 2013

A second look at the Tethyan limbed snakes

Artist's reconstruction of Pachyrhachis problematicus.
Three fossil marine snakes with hind-limbs Pachyrhachis problematicus, Eupodophis descouensi, and Haasiophis terrasanctus. are known from the upper Cretaceous (Cenomanian) of the Middle East. All of them were collected from the region that formed the ancient Tethys Sea. The first species was described in 1979 and a reduced limb lizard,but later recognized as a snake, the others were described in 2000. The phylogenetic status of these snakes has been controversial. In a new paper Palci et al. (2013) have re-evaluated the fossil anatomy of these three species and have drawn some interesting conclusions.  They found no evidence of a laterosphenoid in Haasiophis and Eupodophis; Pachyrhachis and Eupodophis retain a jugal; Haasiophis and Eupodophis, have  chevron bones in the tail; Haasiophis has a large number of unfused intercentra along the anterior portion of the body's vertebral column; and Pachyrhachis has numerous mental foramina on the dentary, as well as at least one sacral vertebra with unfused sacral ribs.

 The authors ran three phylogenetic analyses using alternative out groups (varanoids; iguanians; and skinks+ amphisbaenids, + dibamids) to polarize the character transformations. The in-group consisted of all well-preserved fossil snakes from the Cretaceous, the madtsoiids (mostly Gondwanan snakes with a fossil record extending from the Upper Cretaceous to late Pleistocene from South America, Africa, India, Australia and Southern Europe), and taxa that are representative of all major groups of living snakes. The analyses suggested Pachyrhachis, Eupodophis, and Haasiophis are either a series of stem taxa at the base of the radiation of snakes, or they are members of a clade of fossil snakes that are the sister group to all living alethinopidians (all living snakes minus the scolecophidians).

The authors also found  free intercentra located at the base of the anterior pre-cloacal vertebrae of Haasiophis terrasanctus. If these intercentra are homologous with the cervical intercentra of limbed squamates, this would suggest snakes experienced a considerable amount of axial elongation that involved not only the dorsal but also the cervical region, a point that is supported by the posterior extension of some cervical muscles in snakes. Of interest, a similar pattern of axial elongation as been observed  in dolichosaurs, adriosaurs, and pontosaurs—a group of lizards that have been considered close relatives of snakes since the 19th century. The authors comment that they do not consider these lizards ancestral to snakes, but they may have a close phylogenetic relationship with them.

Alessandro Palci , Michael W. Caldwell and Randall L. Nydam (2013) Reevaluation of the anatomy of the Cenomanian (Upper Cretaceous) hind-limbed marine fossil snakes Pachyrhachis, Haasiophis, and Eupodophis. Journal of Vertebrate Paleontology, 33:6, 1328-1342.

Monday, November 25, 2013

New species of Neotropical Treerunners in the genus Plica

Treerunners are diurnal, medium sized lizards that sit in the open on vertical surfaces, and are often in small colonies that include adults of both sexes and juveniles. The sounds they make scurrying on the bark of trees or rock outcrops draws attention to their presence and thus, they are common in museum collections.

The tropidurid lizard genus Plica (treerunners) currently contains four species restricted to South America east of the Andes. Two of these are relatively widespread (Plica plica and P. umbra). The other two species are associated with Pantepuis. Plica lumaria is known only from southern Venezuela’s Guaiquinima Tepui, and P. pansticta  from the Yutajé–Corocoro massif of Amazonas, Venezuela.

 Etheridge (1970) restricted the type locality for Lacerta plica Linnaeus to the vicinity of Paramaribo, Suriname, designating NRM.112 as the lectotype. Hoogmoed (1973) further restricted the locality to the confluence of the Cottica River and Perica Creek, Suriname. However, the collared treerunner, Plica plica, is known from the countries of Bolivia, Brazil, Colombia, Ecuador, Guyana, Peru, Suriname, and Venezuela, as well as the islands of Trinidad and Tobago, and including the Bocas Island group Additionally, two specimens collected in the 19th century in the British Museum with the locality data “Grenada.”

Of the four species of Plica currently recognized only P. umbra lacks tufts of spines on the neck; and it has 43–69 scales around mid-body. Plica lumaria is black, the superciliaries are directed laterally, it lacks clusters of spines on the fold below the auditory meatus, and it has 141–156 rows of scales around mid-body and 27–33 lamellae under the fourth toe. Plica pansticta has 143–164 scales around mid-body and 31–39 lamellae under the fourth toe. However, P. plica (sensu Etheridge 1970) has 92–202 scales around mid-body; 21–35 lamellae on the fourth finger and 28–45 lamellae on the fourth toe. The polytypic P. plica has been the subject of ecological, morphological, and phylogenetic studies.

Murphy and Jowers (2013) took another look at Plica plica and uncovered multiple species that have been overlooked. While they focused their work on noethern South America, they did examine specimens from across the distyribution of Plica plica and estimate it contains at least 10 species, four of which are described in the new paper published in ZooKeys.

Caption. (a) Plica caribena sp. n. named for its Caribbean coastal distribution. Photo JCM; (b) Plica rayi named in honor of Ray Pawley for his life long work and interest in herpetology. Photo Zelimir Cernelic; (c) Plica plica. Photo Cesar Barrio Amoros; (d) Plica medemi named after Colombian herpetologist and collector of the specimen Fredico Medem. Photo JCM (e) Plica kathleenae named in honor of Kathleen Kelly, Division of Reptiles, Field Museum. Photo JCM.
The allopatric species described in the paper are associated with northern South American geography. Plica plica is associated with the Guiana Shield (Suriname, Guyana and Venezuela). A second species, P. caribeana sp. n. is associated with the Caribbean Coastal Range of Venezuela including Trinidad and Tobago. A third, very distinctive species, P. rayi sp. n. is associated with the Middle Orinoco at the eastern edge of the Guiana Shield.  Two other species, P. kathleenae sp. n. and P. medemi sp. n., are each based upon a single specimen, one from the Sierra Acarai Mountains of Guyana, and the other from southern Meta, Colombia. In addition to the morphological analyses, they sequenced 12S and 16S rDNA gene fragments from one Plica plica from Trinidad to assess its relationship and taxonomy to other mainland Plica. The results suggest Plica caribeana sp. n. likely diverged prior to the separation of Trinidad from Northern Venezuela. Isolation in the Caribbean Coastal Range during its rapid uplift in the late Miocene, combined with a marine incursion into northern Venezuela may have contributed to their genetic divergence from other populations.

Murphy JC, Jowers M. 2013. Treerunners, cryptic lizards of the Plica plica group (Squamata, Sauria, Tropiduridae) of northern South America. ZooKeys

Saturday, November 23, 2013

New study reports US frogs have relatively few abnormalities

A 10-year study shows some good news for frogs and toads on national wildlife refuges. The rate of abnormalities such as shortened or missing legs was less than 2 percent overall — indicating that the malformations first reported in the mid-1990s were rarer than feared. But much higher rates were found in local "hotspots," suggesting that where these problems occur they have local causes. The results were published Nov. 18 in the journal PLOS ONE.

"We now know what the baseline is and the 2 percent level is relatively good news, but some regions need a deeper look," said Marcel Holyoak, professor of environmental science and policy at the University of California, Davis, and a co-author on the study. Hotspot regions included the Mississippi River Valley, California and south-central and eastern Alaska.

Mari Reeves, a graduate student working with Holyoak, led the data analysis and is corresponding author on the paper. Reeves now works at the U.S. Fish and Wildlife Service in Alaska.

Fieldwork for the study was carried out by the Fish and Wildlife Service at 152 refuges across the country between 2000 and 2009. Researchers collected more than 68,000 frogs and toads for the study. The complete dataset is available to researchers and the public online.

The aim of the study was to understand where and when these abnormalities occur — are they widespread, or localized? Are they persistent, or do they appear and fade away? — rather than to identify specific causes, Holyoak said. Understanding the patterns of these hotspots in space and time can help researchers home in on likely causes, he said.

The results show that abnormality hotspots occur in specific places, but within these hotspots the rate of malformations can change over time, Holyoak said.

"We see them at an elevated frequency one year or for a few years, and then they recover," he said.

The most common problems observed were missing or shortened toes or legs, and skin cysts. Only 12 cases of frogs with extra legs were found.

Many different potential causes have been put forward for the abnormalities, including pollution from industry or agriculture, parasites, ultraviolet exposure and naturally occurring heavy metals leaching into water bodies. The exact cause may vary from place to place, Holyoak noted.

The study comes against a background of a general decline in amphibian populations both in the U.S. and worldwide. For example, the California red-legged frog celebrated by Mark Twain's story is now listed as threatened. Frogs and toads may be especially sensitive to changes in climate and air or water quality. It's not clear whether hotspots of malformations contribute to this general decline, Holyoak said, but the new dataset will help researchers explore the problem.

Mari K. Reeves, Kimberly A. Medley, Alfred E. Pinkney, Marcel Holyoak, Pieter T. J. Johnson, Michael J. Lannoo. Localized Hotspots Drive Continental Geography of Abnormal Amphibians on U.S. Wildlife Refuges. PLoS ONE, 2013; 8 (11): e77467 DOI: 10.1371/journal.pone.0077467

Friday, November 22, 2013

Rhinoderma & Bd

Rhinoderma darwinnii. (Photo Credit:
Copyright Claudio Soto-Azat)
Deadly amphibian disease chytridiomycosis has caused the extinction of Darwin's frogs, believe scientists from the Zoological Society of London (ZSL) and Universidad Andrés Bello (UNAB), Chile.
Although habitat disturbance is recognised as the main threat to the two existing species of Darwin's frogs (the northern Rhinoderma rufum endemic to Chile, and the southern Rhinoderma darwinii from Chile and Argentina), this cannot account for the plummeting population and disappearance from most of their habitat.
Conservation scientists found evidence of amphibian chytridiomycosis causing mortality in wild Darwin's frogs and linked this with both the population decline of the southern Darwin's frog, including from undisturbed ecosystems and the presumable extinction of the Northern Darwin's frog.

The findings were published 20 Nov in the journal PLOS ONE.

Professor Andrew Cunningham, from ZSL's Institute of Zoology says: "Only a few examples of the "extinction by infection" phenomenon exist. Although not entirely conclusive, the possibility of chytridiomycosis being associated with the extinction of the northern Darwin's frog gains further support with this study."

Hundreds of specimens of Darwin's frogs and other amphibians from similar habitats collected between 1835 and 1989 were tested in order to find DNA pieces of Batrachochytrium dendrobatidis (Bd), a fungus that causes the disease chytridiomycosis. In addition, 26 populations of Darwin's frogs were surveyed in Chile and Argentina between 2008 and 2012 for the presence of Bd.

Darwin's frogs were named after Charles Darwin who first discovered R. darwinii in 1834 in south Chile during his famous voyage around the globe. The species have a distinct appearance, having evolved to look like a leaf, with a pointy nose. Research leader Dr. Claudio Soto-Azat, from UNAB and former ZSL PhD student says: "Amphibians have inhabited the earth for 365 million years, far longer than mammals. We may have already lost one species, the Northern Darwin's frog, but we cannot risk losing the other one. There is still time to protect this incredible species," Dr Soto-Azat added.

Amphibians provide an important ecosystem service by maintaining balance in the environment. Without them insect plagues and their subsequent effect on agriculture and public health would be more frequent. ZSL scientists are working to further understand the reasons behind the extinction of Darwin's frogs, and ensure the long-term survival of the species.

Claudio Soto-Azat, Andrés Valenzuela-Sánchez, Barry T. Clarke, Klaus Busse, Juan Carlos Ortiz, Carlos Barrientos, Andrew A. Cunningham. Is Chytridiomycosis Driving Darwin’s Frogs to Extinction? PLoS ONE, 2013; 8 (11): e79862 DOI: 10.1371/journal.pone.0079862

Monday, November 18, 2013

Stretching the lower jaw

The ability of skin and organs to stretch is important in determining the size of prey a snake can swallow. Snake skin consists of a keratinized epidermis divided into thick scale regions and thinner, folded interscale regions that are underlain by a dermis containing a complex array of fibrous connective tissues. In a new study Close and Cundall (2013)  examine the skin of the lower jaw of the northern watersnake, Nerodia sipedon, to determine how skin morphology changes when it is highly stretched during ingestion of large prey.

Biomechanical properties of connective tissue have been relatively well studied and collagen is responsible for much of the skin's ability to resist mechanical failure. In mammalian skin, at low levels of strain (up to about 20%) there is little change in the tissue's mechanical properties because collagen undergoes reorientation prior to stretching and slippage. At increased loads collagen account for skin's viscoelastic properties. However, under prolonged periods of strain, collagen alone is incapable of full recovery from high levels of extension due to irreversible creep. Elastin in the deep dermis has been suggested as being responsible  for skin's elastic behavior, but this has not been supported by in vivo or in vitro studies of mammalian skin. Given the known structure and function of elastin it is likely that elastin in the dermis of snakes is responsible for the refolding of interscale skin and subsequently for returning the skin to its resting condition after prolonged periods of stretch.

The skin and intermandibular soft tissues determine the lower jaw's extensibility and the upper jaws of snakes are limited in the degree to which they can move laterally. Therefore, suspensorial length and mobility, mandible length and lower jaw extensibility are the major determinants of gape size in snakes. Within the context of macrostomy - snakes being able to swallow exceptionally large prey - Cose and Cundall (2013)  examine how snake skin between the two sides of the lower jaw behaves during swallowing and how its function is related to structure.

Video records of skin behavior in the lower jaw of watersnakes feeding on fish or anesthetized watersnakes being stretched on an Instron machine showed that most skin extension involves the interscale skin. The largest intermandibular separation recorded during feeding was 7.7x the resting distance, but intermandibular separation reached 10x without tissue failure during mechanical testing. Histological and anatomical analyses of lower jaws fixed in resting, moderately or highly stretched conditions showed that stretching had little effect on scale regions of the epidermis. However, stretching flattened folds of interscale regions at both gross and cellular levels and imposed changes in epidermal cell shape. Stretching of the dermis is primarily limited to realignment of collagen and stretching of elastin in the deep dermis. The configuration of dermal elastin suggests a model for passive recovery of epidermal folding following release of tension.

Close M, Cundall D. 2013. Snake lower jaw skin: Extension and recovery of a hyperextensible keratinized integument. J. Exp. Zool. 9999A:1–20.

Tuesday, November 5, 2013

Snakes control blood flow to the spectacle to improve vision

Instead of eyelids, snakes have a clear scale 
called a spectacle. It works like a window, covering 
and protecting their eyes. When presented with a 
threat, the fight-or-flight response changes the spectacle’s
 blood flow pattern, reducing blood flow for longer 
periods than at rest, up to several minutes.
Nov. 4, 2013 — A new study from the University of Waterloo shows that snakes can optimize their vision by controlling the blood flow in their eyes when they perceive a threat.

Kevin van Doorn, PhD, and Professor Jacob Sivak, from the Faculty of Science, discovered that the coachwhip snake's visual blood flow patterns change depending on what's in its environment. The findings appear in the most recent issue of the Journal of Experimental Biology.

"Each species' perception of the world is unique due to differences in sensory systems," said van Doorn, from the School of Optometry & Vision Science.

Instead of eyelids, snakes have a clear scale called a spectacle. It works like a window, covering and protecting their eyes. Spectacles are the result of eyelids that fuse together and become transparent during embryonic development.

When van Doorn was examining a different part of the eye, the illumination from his instrument detected something unusual.

Surprisingly, these spectacles contained a network of blood vessels, much like a blind on a window. To see if this feature obscured the snake's vision, van Doorn examined if the pattern of blood flow changed under different conditions.

When the snake was resting, the blood vessels in the spectacle constricted and dilated in a regular cycle. This rhythmic pattern repeated several times over the span of several minutes.

But when researchers presented the snake with stimuli it perceived as threatening, the fight-or-flight response changed the spectacle's blood flow pattern. The blood vessel constricted, reducing blood flow for longer periods than at rest, up to several minutes. The absence of blood cells within the vasculature guarantees the best possible visual capacity in times of greatest need.

"This work shows that the blood flow pattern in the snake spectacle is not static but rather dynamic," said van Doorn.

Next, the research team examined the blood flow pattern of the snake spectacle when the snake shed its skin. They found a third pattern. During this time, the vessels remained dilated and the blood flow stayed strong and continuous, unlike the cyclical pattern seen during resting.

Together, these experiments show the relationship between environmental stimuli and vision, as well as highlight the interesting and complex effect blood flow patterns have on visual clarity. Future research will investigate the mechanism underlying this relationship.

"This research is the perfect example of how a fortuitous discovery can redefine our understanding of the world around us," said van Doorn.

K. van Doorn, J. G. Sivak. Blood flow dynamics in the snake spectacle. Journal of Experimental Biology, 2013; 216 (22): 4190 DOI: 10.1242/jeb.093658