Tuesday, November 10, 2015

The evolution of venom, a new perspective

This is an Anderson's Pitviper (Trimeresurus andersoni), a venomous 
snake in the Andaman Islands of India. Photo Credit: Dr. Kartik Sunagar

In a new study published in  PLOS Genetics, scientists at the Hebrew University of Jerusalem have revealed new discoveries about the evolution of venom. The research points to a 'two-speed' evolution of animal venom, showing for the first time the significant roles played by different forces of natural selection.

Venom is a complex mixture of proteins and other toxic chemicals produced by animals such as snakes and spiders, either to incapacitate their prey or to defend against predators. The influence of positive selection (the process by which a protein changes rapidly over evolutionary time scales) in expanding and diversifying animal venoms is widely recognized.

This process was hypothesized to result from an evolutionary chemical arms race, in which the invention of potent venom in the predatory animals and the evolution of venom resistance in their prey animals, exert reciprocal selection pressures.

In contrast to positive selection, the role of purifying selection (also known as negative selection, which is the selective removal of deleterious genetic changes from a population) has rarely been considered in venom evolution.

Moreover, venom research has mostly neglected ancient animal groups in favor of focusing on venomous snakes and cone snails, which are both "young" animal groups that originated only recently in evolutionary timescales, approximately 50 million years ago. Consequently, it was concluded that venom evolution is mostly driven by positive selection.

In the new study, Dr. Yehu Moran at the Hebrew University's Department of Ecology, Evolution and Behavior and the guest scientist Dr. Kartik Sunagar examined numerous venom genes in different animals in order to unravel the unique evolutionary strategies of toxin gene families.

The researchers analyzed and compared the evolutionary patterns of over 3500 toxin sequences from 85 gene families. These toxins spanned the breadth of the animal kingdom, including ancient venomous groups such as centipedes, scorpions, spiders, coleoids (octopus, cuttlefish and squids) and cnidarians (jellyfish, sea anemones and hydras).

Unexpectedly, despite their long evolutionary histories, ancient animal groups were found to have only accumulated low variation in their toxins.

The analysis also revealed a striking contrast between the evolution of venom in ancient animal groups as compared to evolutionarily "young" animals. It also highlighted the significant role played by purifying selection in shaping the composition of venoms.

According to Dr. Yehu Moran, "Our research shows that while the venoms of ancient lineages evolve more slowly through purifying selection, the venoms in more recent lineages diversify rapidly under the influence of positive selection."

The findings enable the postulation of a new theory of venom evolution. According to this theory, toxin-producing genes in young venomous groups that enter a novel ecological niche, experience a strong influence of positive selection that diversifies their toxins, thus increasing their chances to efficiently paralyze relevant prey and predatory species in the new environment.

However, in the case of the ancient venomous groups, where the venom is already "optimized" and highly suitable for the ecological niche, the venom's rate of accumulating variations slows down under the influence of purifying selection, which preserves the potent toxins generated previously.

The proposed "two-speed" mode of venom evolution highlights the fascinating evolutionary dynamics of this complex biochemical cocktail, by showing for the first time the significant roles played by different forces of natural selection in shaping animal venoms.

According to Drs. Moran and Sunagar, "The 'two-speed' mode of evolution of animal venoms involves an initial period of expansion, resulting in the rapid diversification of the venom arsenal, followed by longer periods of purifying selection that preserve the now potent toxin pharmacopeia. However, species that have entered the stage of purification and fixation may re-enter the period of expansion if they experience a major shift in ecology and/or environment."


Kartik Sunagar & Yehu Moran. The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals. PLOS Genetics, 2015; 11 (10): e1005596 DOI: 10.1371/journal.pgen.1005596

Sunday, November 8, 2015

The origin of large body size and herbivory in giant Canary Island lacertids

Gallotia galloti. Photographer's Credit: Petermann
2005, via Wikimedia Commons
The Island Rule on body size claims big animals  evolve smaller body sizes due to the limited resource of food and limited habitat; while smaller animals that have no natural enemies in islands evolve larger body sizes.

 Andrej Čerňanský and colleagues discovered a fossil related to the genus Gallotia which is endemic to the  Canary Islands. They named it Janosikia ulmensis, after the Slovak national hero, outlaw Juraj Jánošík. Zoological Journal of the Linnean Society reports the results. The genus Gallotia has not been growing in size on the island – quite the contrary. The Gallotia ancestor came to the island with a large body size.

Until now, the genus Gallotia was considered a clear example of island gigantism; scientists supposed that a small lizard resembling the North African species Psammodromus colonised the Canary islands 20 to 18 million years ago. As it did not have any natural enemies, it supposedly gradually increased its body size several times. But the fossil record illustrating this  was absent.

“Currently, we have been able to do research, for the first time, on fossils and almost complete findings from about 22 million years old which are in the line leading to the lizards from the Canary Islands. Our fossil comes from Germany and precedes the period of the islands’ colonisation. It also shows us a completely different story, proving that the evolution of body size is much more complex than we had originally thought,” Čerňanský explained.

This stems from a whole set of anatomic features – like the huge size, as the skull alone was almost five centimetres long, the Slovak researcher said. This shows that this line had already grown to this size on the continent before colonising the islands; some other current species from the islands, on the other hand, represent markedly smaller animals. Thus, Janosikia turned the original idea upside down.

The fossil is crucial for understanding the island rule of evolution of body size, and also the herbivory of today’s large species of lizards. It also confirms the assumption of molecular biologists that the line leading to the genus Gallotia has its origin on the European continent; and, last but not least, it is one of the best preserved lizards from the Tertiary that reveals many important, so far unknown aspects of the evolution of dominant group of reptiles in Europe – the family Lacertidae, Čerňanský summed up.

Janosikia ulmensis is from the early Miocene of Ulm, Germany (∼22 Mya). The authors show that this species and the Oligocene Pseudeumeces cadurcensis (Filhol, 1877) are in fact crown lacertids, and the first known pre-Quaternary record of the total clade of Gallotia. Pseudeumeces confirms the early origin of crown Lacertidae in the Palaeogene of Europe. More importantly, these fossil taxa show that large body size was already achieved on the European mainland by the early Miocene. Furthermore, Pseudeumeces and Janosikia were faunivorous, thus demonstrating that insularity, not large body size, was crucial to the evolution of herbivory in this lineage. Body size change in Gallotia was more complex than previously thought, encompassing size increase [e.g. in the extinct Gallotia goliath (Mertens, 1942)], but more commonly involving miniaturization. The physical environment may play a crucial role in modulating the evolution of body size.

Čerňanský, A., Klembara, J. and Smith, K. T. (2015), Fossil lizard from central Europe resolves the origin of large body size and herbivory in giant Canary Island lacertids. Zoological Journal of the Linnean Society. doi: 10.1111/zoj.12340.

Friday, October 30, 2015

The diet of Gasperetti’s sand viper

By Zuhair Amr via Wikimedia Commons
Gasperetti’s sand viper, Cerastes gasperetti, is the most common snake in Saudi Arabia. However, this snake remains poorly studied. It is distributed throughout many deserts in Egypt, Jordan and Saudi Arabia. Horned viper is a nocturnal, true desert snake and prefers sandy soil with some vegetation. Horned vipers are generally considered opportunistic predators with varied diets. However no study has specifically addressed the diet of Cerastes gasperettii.  Al-Sadoom et al. (2015) examined 238 specimens from Al-Thumama area, in the central region of Saudi Arabia collected over a period of one year May, 1998 – April, 1999. The digestive system was examined. Eighty specimens of both sexes were studied for gut content analysis. They found larger specimens of Gasperetti’s sand viper feeds mostly on rodents (Gerbillus cheesmani and Mus musculus) which were found in snakes with larger size and formed 70% of the stomach contents. Arthropods (beetles) constituted 15% of the contents and lizards (Acanthodactylus schmiditi and Stenodactylus slevinii) form 10% of the total diet. The remaining 5% of the stomach content was completely digested and could not be identified.

Al-Sadoon, M. K., & Paray, B. A. (2015). Ecological Aspects of the Horned viper, Cerastes cerastes gasperettii in the Central Region of Saudi Arabia. Saudi Journal of Biological Sciences.

Wednesday, October 14, 2015

The Cuban Racer in the Bahamas

Cubophis cantherigerus cantherigerus. Photo by Lisa Ferguso
Dipsadidae is one of the largest snake families with more than 754 species, mostly distributed in the Neotropics. The subfamily Xenodontinae is exclusive to South American to Mexico and the West Indies. Mexico, and the West Indies, and highly diverse in both morphology and natural history. The Tribe Alsophiini holds about 43 species restricted to the West Indies. These are typically slender, fast-moving, and active diurnal foragers often commonly called racers. While taxonomic classifications of xenodontines were historically based on hemipenial, dentition, external morphology, and color pattern, recent molecular analyses of Alsophiini are not necessarily in agreement regarding monophyly of the group In 2012, Krysto et al. (2015) collected the first known dipsadid snake on the Cay Sal Bank, The Bahamas. Only two snake species have been previously recorded from any island on the Cay Sal Bank: the Bahamian Slender Blindsnake, Typhlops biminiensis, on Elbow Cay; and the Northern Bahamas Trope, Tropidophis curtus (Garman 1887), on both Elbow Cay and Double Headed Shot Cay.

Krysto et al. examine the external morphology, dentition, and color pattern, and conduct molecular analyses of Caribbean Alsophiine snakes to determine the species identity and phylogenetic placement of the Cay Sal Bank snake. They analyze 3,426 base pairs (bp) of sequence data derived from five mitochondrial loci and one nuclear locus using Maximum Likelihood (ML) and Bayesian Inference (BI) methods. Our molecular data agree with some aspects of morphology (e.g., scale counts, dentition, and color pattern) supporting identification of this specimen as the Cuban Racer, Cubophis cantherigerus cantherigerus (Bibron 1840), a species previously regarded as endemic to Cuba. This discovery provides another example of the strong Cuban affinities of the terrestrial vertebrate fauna of the Bahamian islands.

KRYSKO, K. L., STEADMAN, D. W., NUÑEZ, L. P., & LEE, D. S. (2015). Molecular phylogeny of Caribbean dipsadid (Xenodontinae: Alsophiini) snakes, including identification of the first record from the Cay Sal Bank, The Bahamas. Zootaxa, 4028(3), 441-450.

Wednesday, September 30, 2015

New Book, Natural History of Neotropical Treeboas (genus Corallus)

Nine species comprise the arboreal boid genus Corallus. Combined, they range from Guatemala in northern Central America to southeastern Brazil in South America, and two species occur on islands in the West Indies. Based on extensive fieldwork by the author extending over 25 years, observations from colleagues, and the literature, Natural History of Neotropical Treeboas (Genus Corallus) summarizes, often in great detail, our current knowledge of treeboa habitats, activity, diet, foraging strategies, defensive behaviors, predators, reproduction, population characteristics, and the shared history of humans and treeboas and the impact humans have had on treeboa natural history. In addition to more than 270 photos depicting treeboa color variation, habitats, predation, and mating, Natural History of Neotropical Treeboas (Genus Corallus) also includes maps, numerous graphs, 26 tables, and more than 400 literature references.

"Robert W. Henderson has conducted research on Neotropical treeboas for nearly 25 years, elucidating aspects of their natural history and monitoring changes in populations over time, emphasizing in particular how these snakes have adjusted in light of human-mediated changes to their habitat, prey base, and predators. In this book, Henderson provides insights into habitat, activity, diet and foraging, predators and defense, and reproduction, with each chapter providing insights, a large percentage of them firsthand, into what we know about these intriguing snakes. I take great pride in seeing a boa before Bob does (it happens rarely), but then he has undoubtedly encountered more treeboas in their natural habitat than anyone."
– Robert Powell

Saturday, September 26, 2015

Fluctuating sea levels and global cooling reduced crocodylian species over millions of years

The giant Sarcosuchus, an extinct crocodilian. Illustrators Credit: Imperial
 College London and Robert Nicholls (Paleocreations)
Crocodylians include present-day species of crocodiles, alligators, caimans and gavials and their extinct ancestors. Crocodylians first appeared in the Late Cretaceous period, approximately 85 million years ago, and the 250 million year fossil record of their extinct relatives reveals a diverse evolutionary history.

Extinct crocodylians and their relatives came in all shapes and sizes, including giant land-based creatures such as Sarcosuchus, which reached around 12 metres in length and weighed up to eight metric tonnes. Crocodylians also roamed the ocean -- for example, thalattosuchians were equipped with flippers and shark-like tails to make them more agile in the sea.

Many crocodylians survived the mass extinction that wiped out almost all of the dinosaurs 66 million years ago, but only 23 species survive today, six of which are classified by the International Union for Conservation of Nature as critically endangered and a further four classified as either endangered or vulnerable.

In a new study published in Nature Communications, researchers from Imperial College London, the University of Oxford, the Smithsonian Institution and the University of Birmingham compiled a dataset of the entire known fossil record of crocodylians and their extinct relatives and analysed data about Earth's ancient climate. They wanted to explore how the group responded to past shifts in climate, to better understand how the reptiles may cope in the future.

Crocodylians are ectotherms, meaning they rely on external heat sources from the environment such as the Sun. The researchers conclude that at higher latitudes in areas we now know as Europe and America, declining temperatures had a major impact on crocodylians and their relatives.

At lower latitudes the decline of crocodylians was caused by areas on many continents becoming increasingly arid. For example, in Africa around ten million years ago, the Sahara desert was forming, replacing the vast lush wetlands in which crocodylians thrived. In South America, the rise of the Andes Mountains led to the loss of a proto-Amazonian mega wetland habitat that crocodylians lived in around five million years ago.

Marine species of crocodylians were once widespread across the oceans. The team found that fluctuations in sea levels exerted the main control over the diversity of these creatures. For example, at times when the sea level was higher it created greater diversity because it increased the size of the continental shelf, providing the right conditions near the coast for them and their prey to thrive.

Interestingly, the Cretaceous-Paleogene mass extinction event, which wiped out many other creatures on Earth nearly 66 million years ago including nearly all of the dinosaurs, had positive outcomes for the crocodylians and their extinct relatives. The team found that while several groups did go extinct, the surviving groups rapidly radiated out of their usual habitats to take advantage of territories that were now uninhabited.

In the future, the team suggest that a warming world caused by global climate change may favour crocodylian diversification again, but human activity will continue to have a major impact on their habitats.

Dr Philip Mannion, joint lead author from the Department of Earth Science and Engineering at Imperial College London, said: "Crocodylians are known by some as living fossils because they've been around since the time of the dinosaurs. Millions of years ago these creatures and their now extinct relatives thrived in a range of environments that ranged from the tropics, to northern latitudes and even deep in the ocean. However, all this changed because of changes in the climate, and crocodylians retreated to the warmer parts of the world. While they have a fearsome reputation, these creatures are vulnerable and looking back in time we've been able to determine what environmental factors had the greatest impact on them. This may help us to determine how they will cope with future changes."

The next step for the researchers will be for them to look at similar patterns in other fossil groups with long histories, such as mammals and birds to determine how past climate influenced them.


Philip D. Mannion, Roger B. J. Benson, Matthew T. Carrano, Jonathan P. Tennant, Jack Judd, Richard J. Butler. Climate constrains the evolutionary history and biodiversity of crocodylians. Nature Communications, 2015; 6: 8438 DOI: 10.1038/ncomms9438

Friday, September 25, 2015

Snakebite, Economics, and El Nino in Costa Rica

Snakes and snakebites in Costa Rica. (A) The terciopelo 
B. asper. (B) Average annual snakebite incidence, by 
canton, from 2005 to 2013. County color indicates snakebite
incidence rate, county boundary color indicates relative risk, 
and a marking described in the map legend indicates the 
primary cluster. From Chaves et al. 2015
Snake envenomation is frequently considered a neglected medical problem in rural, tropical or subtropical populations. In a new paper Chaves et al. (2015) examine how climate change's impact on snake ecology could influence the incidence of snakebites. They asked whether snakebites reported in Costa Rica between 2005 and 2013 were associated with meteorological fluctuations. The El Niño Southern Oscillation (ENSO) is a climatic phenomenon associated with cycles of other neglected tropical diseases. They examine how spatial heterogeneity in snakebites and poverty are associated, given the importance of poverty in other neglected tropical diseases.

The authors found that periodicity in snakebites reflects snake reproductive phenology and is associated with ENSO. Snakebites are more likely to occur at high temperatures and may be significantly reduced after the rainy season. Nevertheless, snakebites cluster in Costa Rican areas with the heaviest rainfall, increase with poverty indicators, and decrease with altitude. Altogether, our results suggest that snakebites might vary as a result of climate change.

Chaves et al. found 6424 snakebites were reported in Costa Rica from 2005 to 2013. The 9-year average incidence rate was 15.24 per 100,000, ranging from 10.63 per 100,000 to 22.98 per 100,000 when the entire population was assumed to be at risk. However, those statistics underestimate the incidence rate in the at-risk population which is mainly rural. The average rate jumps to 41.27 per 100,000, ranging from 30.53 per 100,000 to 58.94 per 100,000 with a steadily decreasing at-risk population. The highest incidence of bites occurred in southern Costa Rica and in the northern portion of La Cruz, bordering Nicaragua. Snakebites usually occurred in suburban or rural regions.
The study shows that snakebites are associated with changes in temperature and rainfall across time, and that unusually high numbers of snakebites occur during the cold and hot phases of ENSO. Spatially, snakebites cluster in the most humid lowland areas of Costa Rica, where terciopelos (Bothrops asper)  are common, and are more frequent in the economically poorest areas with similar weather patterns. This combination of patterns highlights the fact that snakebites follow meteorological changes, and these patterns  reflect the impact of meteorological fluctuations on snake biology.

Snakebites follow a common pattern seen in other tropical diseases in the region and reflecting the general vulnerability of impoverished human populations to the adverse effects of climate change and neglected diseases. The latter is a pattern that might be extrapolated to other areas where snakebites are a major health problem. The findings highlight the need for increased research on the eco-epidemiology of snakebites, a neglected tropical disease that should be included in the list of diseases or health hazards that are sensitive to environmental changes.

Chaves, L. F., Chuang, T. W., Sasa, M., & Gutiérrez, J. M. (2015). Snakebites are associated with poverty, weather fluctuations, and El Niño. Science Advances, 1(8), e1500249.

Large monitor lizards and early Australians

At least three large species of monitor lizards lived in prehistoric Australia, an undescribed fossil species known from one location, the Komodo dragon (Varanus  komodoensis), and the Megalania (Varanus priscus). Komodo dragons are an extant relic species confined to a few islands in the Lesser Sundas, Indonesia.  Megalania is extinct, attained a length of about 7 m and like other Varanus probably had a venomous bite.  Megalania remains have been excavated from five locations.  Humans arrived in Australia about 50,000 years ago and the megalania remains from two sites may be less than 50,000 years old, but the dating at these sites has been considered unreliable.  In a new paper, Price et al. (2015) report remains of giant monitor that overlapped with the humans.

As if life wasn't hard enough during the last Ice Age, research led by the University of Queensland has found Australia's first human inhabitants had to contend with giant killer (=monitor) lizards.

UQ vertebrate palaeoecologist Dr Gilbert Price said researchers working in Central Queensland were amazed when they unearthed the first evidence that Australia's early human inhabitants and giant apex predator lizards had overlapped.

"Our jaws dropped when we found a tiny fossil from a giant lizard during a two metre deep excavation in one of the Capricorn Caves, near Rockhampton," Dr Price said.

"The one-centimetre bone, an osteoderm, came from under the lizard's skin and is the youngest record of a giant lizard on the entire continent."

Dr Price and his colleagues used radiocarbon and uranium thorium techniques to date the bone as about 50,000 years old, coinciding with the arrival of Australia's Aboriginal inhabitants.

"We can't tell if the bone is from a Komodo dragon -- which once roamed Australia -- or an even bigger species like the extinct Megalania prisica, which weighed about 500 kg and grew up to six metres long," Dr Price said.

"The find is pretty significant, especially for the timeframe that it dates."

The largest living lizard in Australia today is the perentie, which can grow up to two metres long.

Dr Price, from UQ's School of Earth Sciences, said massive lizards and even nine-metre long inland crocodiles roamed Australia during the last Ice Age in the Pleistocene geological period.

"It's been long-debated whether or not humans or climate change knocked off the giant lizards, alongside the rest of the megafauna," he said.

"Humans can only now be considered as potential drivers of their extinction."

The bone was found in what could be Australia's most fossil-rich site, with the Capricorn Caves housing millions of bones of many species.

Dr Price said scientists could only hypothesise how the giant lizard bone made its way inside the cave, which contains bones of many rodents regurgitated by owls.

He said a crew of volunteer citizen scientists helped with the research by sorting and sieving specimens.

Capricorn Caves manager Ann Augusteyn said the find highlighted her team's "huge responsibility" to care for the caves.

"This study also begs the question -- what else is entombed in our caves and what else can we learn?"

Price GJ,  Louys J,  Cramb J, Feng Y-X,  Zhao J-X,  Hocknull SA, . Webb GE,  Nguyen AD, Joannes-Boyau R. 2015. Temporal overlap of humans and giant lizards (Varanidae; Squamata) in Pleistocene Australia. Quaternary Science Reviews, 2015; 125: 98 DOI: 10.1016/j.quascirev.2015.08.013

Sunday, September 20, 2015

The cold climate hypothesis and viviparity in snakes

Two neonate Enhydris enhydris emerging from the birth canal at the same time.
Most homalapsid snakes are tropical yet viviparous.
The usual answer to the question of which came first the egg or the neonate in lizards and snakes is usually answered as the egg. Squamates reproduce either by laying eggs (oviparity) or by giving birth to live young (viviparity). Most squamates (about 80–85%) are oviparous, and the reproductive mode is generally phylogenetically constrained [e.g. all homalopsids are considered to be viviparous and all anoles are oviparous. Nonetheless, some families (e.g. Elapidae, Natricidae and Viperidae) and genera (e.g. Eryx, Liolaemus and Pseudechis) contain both viviparous and oviparous species. Transitions between oviparity and viviparity are even present in different populations of the same species (e.g. Zootoca vivipara, Saiphos equalis and Helicops angulatus) although such variability is rare. Oviparity is traditionally considered to be the ancestral mode of squamate reproduction viviparity is thought to have evolved independently in at least 30 lineages of snakes and in more than 100 lineages of squamates, but recently it was suggested that viviparity may have evolved first.
In a forthcoming paper in Global Ecology and Biogeography, Feldman et al. (2015) test two prevailing hypotheses regarding the biogeography of reptile reproductive modes to evaluate the selective forces driving the evolution of viviparity in snakes. The cold climate hypothesis posits that viviparity is selected for in cold climates, whereas the climatic predictability hypothesis predicts that viviparity is advantageous in seasonal climates. They collated detailed distribution maps and reproductive mode data for 2663 species of the world’s terrestrial alethinophidian snakes; studied the relationship between snake reproductive mode and environmental predictors; applied an ecological and an evolutionary approach to study snake reproductive mode by performing the analyses at the assemblage level and species level
Respectively; and analyzed our data at the global and continental scales to learn whether tendencies to viviparity are similar world-wide.
The authors found strong support for the cold climate hypothesis and the assumption that viviparity is an adaptation to cold environments. There was little support for the climatic predictability hypothesis. Nonetheless, viviparous species are not restricted to cold environments. They conclude that viviparity is adaptive in cold climates, but not necessarily in unpredictable/ seasonal climates. Current distributions may not reflect the climate at the time and place of speciation. The authors suggest many viviparous snakes inhabiting warm climates are members of lineages that originated in colder regions, and their occurrence in maladaptive environments is a result of phylogenetic conservatism.

Feldman, A., Bauer, A. M., Castro‐Herrera, F., Chirio, L., Das, I., Doan, T. M., ... & Meiri, S. (2015). The geography of snake reproductive mode: a global analysis of the evolution of snake viviparity. Global Ecology and Biogeography.

Friday, September 18, 2015

New taxonomic arrangement for the short-horned lizards of the douglasii Species Group

Members of the Phrynosma douglassi complex. Photo
 credit: R. Montanucci.
Horned Lizards of the genus Phrynosoma are perhaps the most novel North American lizards. One species group, the Short-horned lizards (the Phrynosoma douglasii species complex) occur throughout the inter-montane West and Great Plains of western North America. In a new paper, Montanucci (2015) has reviewed the taxonomy of these lizards, using comparative morphology and color pattern variation in 3,174 specimens.  Multivariate analyses of 20 morphological and color-pattern characters were applied to 977 specimens, and univariate statistics were summarized for 52 samples totaling 1,134 specimens. The results support the recognition of Phrynosoma douglasii (Bell 1828) as a distinct species, and the resurrection of P. brevirostris Girard 1858 and P. ornatissimum Girard 1858 as species distinct from Phrynosoma hernandesi Girard 1858.
Phrynosoma brevirostris is found in sagebrush and short-grass communities as well as in open canopy conifer savanna at higher elevations. Two new species allied to Phrynosoma brevirostris were described.  Phrynosoma bauri from the eastern plains of Colorado and northeastern New Mexico, southeastern Wyoming and southwestern Nebraska south of the North Platte River inhabits areas dominated by Grama-buffalo grass to Juniper-pinyon woodland, and Pine-Douglas fir. The second species allied to P. brevirostris is Phrynosoma diminutum, a species endemic to the San Luis Valley of southern Colorado and northern New Mexico. The Mexican taxon brachycercum Smith is reassigned as a subspecies of Phrynosoma ornatissimum. The ranges of Phrynosoma hernandesi and P. ornatissimum broadly overlap in central New Mexico, the former occupying the coniferous forests of disjunct mountain ranges, the latter occurring in the surrounding desert grasslands.
Principal components analysis suggests morphological evidence for hybridization where the two taxa meet, often within ecotones between montane forest associations and grasslands. Principal components analysis also revealed a high level of morphological variability in the Colorado Plateau region of northeastern Arizona, northwestern New Mexico, extreme southwestern Colorado and adjacent Utah. The evidence suggests that these populations arose through past hybridization between the two species.
The taxon ornatum Girard 1858, although sharing several traits with Phrynosoma brevirostris, is morphologically close to P. hernandesi. It is regarded as a stabilized population of hybrid origin, but treated as a subspecies of Phrynosoma hernandesi.
Phrynosoma douglasii inhabits Sagebrush steppe over much of the Columbia Plateau of eastern Washington based on museum records. It has been reported only from the sagebrush regions of southeastern Washington. The dense, low to medium tall grass may have precluded the establishment of short-horned lizard populations over much of this habitat, except where exposed, friable soils were present. In Oregon, populations east of the Cascades occur in Sagebrush steppe, but in the vicinities of Lake Abert and Fossil Lake, the lizards have also been collected in Saltbush-greasewood association. In the Cascade Range, populations occur in open conifer forest, including Silver fir-Douglas fir forest and Fir-hemlock forest on the western slopes, and Grand fir-Douglas fir forest, and Ponderosa shrub forest on the eastern slopes above the Sagebrush steppe.
 Phrynosoma douglasii inhabits open-canopy forests with widely spaced trees and well-drained, friable soils. Dense forests, with closed canopies, impede the establishment of populations. In southern Idaho, known localities are dominated by sagebrush steppe, and as yet, there are no confirmed records in Douglas fir forest and Western spruce-fir forest in the mountain ranges north of the Snake River Plain.
Phrynosoma h. hernandesi ranges from northern Sonora (recorded as far south as Sierra de la Madera) through the isolated mountain ranges and grasslands of southeastern Arizona northward along the Mogollon Rim. It ranges across the Coconino and Kaibab plateaus and follows the Wasatch Range in Utah. It occurs in the Pavant Range west of the Sevier River, and in the Henry Mountains northeast of the Escalante River, but presently there are no records from the Uinta Mountains in Utah. In northwestern Arizona there are records for the Hualapai and Cerbat mountains, Shivwits Plateau (near Snap Point) and the Mount Trumbull area.
The taxonomic arrangement in this study, with the exception of P. douglasii, is largely discordant with the proposed taxonomy from a previously published study based on mitochondrial DNA sequence data.


Montanucci, R. R. (2015). A taxonomic revision of the Phrynosoma douglasii species complex (Squamata: Phrynosomatidae). Zootaxa, 4015(1), 1-177.

Monday, September 14, 2015

South Florida and invasive herps

Iguana iguana is invasive in Florida
South Florida is on the front lines in the war against invasive reptiles and amphibians because its warm climate makes it a place where they like to live, a new University of Florida study shows.

Using computer models and data showing where reptiles live in Florida, UF/IFAS scientists predicted where they could find non-native species in the future. They found that as temperatures climb, areas grow more vulnerable to invasions by exotic reptiles. Conversely, they found that extreme cold temperatures protect against invasion.

"Early detection and rapid response efforts are essential to prevent more of the 140 introduced species from establishing breeding populations, and this study helps us choose where to look first," said Frank Mazzotti, a wildlife ecology and conservation professor at the University of Florida Institute of Food and Agricultural Sciences Fort Lauderdale Research and Education Center.

The new study is published online in the journal Herpetological Conservation Biology.

Lead author Ikuko Fujisaki, an assistant professor of wildlife ecology and conservation at the Fort Lauderdale REC, said scientists conducted the study to provide scientific data for managing invasive wildlife in the Sunshine State.

America imports more exotic animals than any other country in the world, with more than 1 billion animals entering the nation from 2005 through 2008, according to the U.S. Government Accountability Office. They come in by boats, planes and other modes of transportation. The animals are often used in the pet trade, but have other uses as well, including food and religious practices. Once they're established, exotic animals are costly to remove, according to a 2010 led by Michigan State University. Therefore, wildlife management agencies are always looking for better ways to detect the invasive species early.

Urban areas are hubs of international transport and therefore are major gateways for exotic pests. With its subtropical and tropical climates and its high human population (19.9 million as of 2014), Florida provides a unique opportunity for a geographic risk assessment because of the number of exotic species that establish, fail to establish or whose fate is unknown, the UF/IFAS scientists said.

Invasive species are second only to losing habitats in contributing to the loss of biodiversity worldwide, Mazzotti wrote in a 2015 UF/IFAS Extension paper. Florida has more introduced species of reptiles and amphibians in the wild than anywhere else in the world.

This data leads Mazzotti to suggest South Florida as the focal area for exotic species.

"We need to focus immediate management efforts on South Florida, or invasive wildlife could jeopardize Everglades restoration," Mazzotti said.

The authors add, "Since we created our list of target species, additional exotic herpetofaunal species have been introduced and become established in Florida. Some institutions in Florida, such as UFHerpetology, have been working toward accurately georeferencing occurrence locations in the state and make the data available online (https://www. flmnh.ufl.edu/herpetology/) or shared with other online databases such as GBIF and HerpNet (http://www.herpnet.org). Such data could be useful to further improve our predictions. Further, numerous imported exotic reptile species have not yet been observed in the wild but could be introduced through various pathways. Previous taxonomic risk assessments of exotic species have proposed various algorithms to predict potentially invasive species and have discussed their utility in invasive species management (Hayes and Barry 2008). Such assessments have been a part of the Australian national screening protocol for plants (Pheloung et al. 1999; Keller et al. 2007) and have been recommended for introduction as a part of invasive management practice in the United States (Lodge et al. 2006). Geographic assessments such as ours can be used to develop cost-effective management strategies by depicting spatial variability in habitat suitability for established, introduced, and imported species over wide geographic areas with variable environmental conditions.


Ikuko Fujisaki, Frank J. Mazzotti, James Watling, Kenneth L. Krysko, and Yesenia Escribano. Geographic Risk Assessment Reveals Spatial Variation in Invasion Potential of Exotic Reptiles in an Invasive Species Hotspot. Herpetological Conservation Biology, 2015; 10 (2): 621-632 

Wednesday, September 9, 2015

Eunotosaurus, and the origin of turtles

Eunotosaurus africanus (Seeley 1892) Middle Permian ~15 cm 
snout to vent length, was considered by Watson (1914) as the 
ancestor to the turtle because of its wide ribs and low number 
of dorsal vertebrae. The present study nests turtles with 
Stephanospondylus and the wide ribs find their origins in the 
less wide ribs of Milleretta RC14. Derived from a sister to
Acleistorhinus, Eunotosaurus left no known descendent taxa.

A research team led by NYIT scientist Gaberiel Bever has determined that a 260-million year-old fossil species found in South Africa's Karoo Basin provides a long awaited glimpse into the murky origins of turtles.

Bever, describes the extinct reptile, named Eunotosaurus africanus, as the earliest known branch of the turtle tree of life.

"Eunotosaurus is a critical link connecting modern turtles to their evolutionary past," said Bever, an assistant professor of anatomy at the NYIT College of Osteopathic Medicine. "This is the fossil for which science has been searching for more than 150 years. You can think of it as a turtle, before turtles had a shell."

While Eunotosaurus lacks the iconic turtle shell, its extremely wide ribs and distinctively circular torso are the first indications that this fossil represents an important clue in a long unsolved mystery: the origin of turtles. In a new study published in Nature, Bever and his colleagues from the Denver Museum of Nature and Science, Yale University, and the University of Chicago focus their attention on the skull of Eunotosaurus. Their findings indicated that the complex anatomy of the head houses convincing evidence of the important role played by Eunotosaurus in the deep history of turtle evolution.

"Our previous studies showed that Eunotosaurus possessed structures that likely represent the first steps in the evolution of the turtle shell" added Tyler Lyson of the Denver Museum of Science and Nature and a coauthor of the study, "but what those studies lacked was a detailed analysis of the skull."

Using high-resolution computed tomography, Bever digitally dissected the bones and internal structures of multiple Eunotosaurus skulls, all of which are housed in South African museums. He then incorporated his observations into a new analysis of the reptile tree of life. The process took the better part of four years, but according to Bever, the results were well worth the effort.

"Imaging technology gave us the opportunity to take the first look inside the skull of Eunotosaurus," said Bever, "and what we found not only illuminates the close relationship of Eunotosaurus to turtles, but also how turtles are related to other modern reptiles."

One of the study's key findings is that the skull of Eunotosaurus has a pair of openings set behind the eyes that allowed the jaw muscles to lengthen and flex during chewing. Known as the diapsid condition, this pair of openings is also found in lizards, snakes, crocodilians, and birds. The skull of modern turtles is anapsid -- without openings -- with the chamber housing the jaw muscles fully enclosed by bone.

The anapsid-diapsid distinction strongly influenced the long-held notion that turtles are the remnants of an ancient reptile lineage and not closely related to modern lizards, crocodiles, and birds. The new data from Eunotosaurus rejects this hypothesis.

"If turtles are closely related to the other living reptiles then we would expect the fossil record to produce early turtle relatives with diapsid skulls," said Bever. "That expectation remained unfulfilled for a long time, but with some help from technology and a lot of hard work on our part, we can now draw the well-supported and satisfying conclusion that Eunotosaurus is the diapsid turtle that earlier studies predicted would be discovered."

In linking turtles to their diapsid ancestry, the skull of Eunotosaurus also reveals how the evidence of that ancestry became obscured during later stages of turtle evolution.

"The skull of Eunotosaurus grows in such a way that its diapsid nature is obvious in juveniles but almost completely obscured in adults. If that same growth trajectory was accelerated in subsequent generations, then the original diapsid skull of the turtle ancestor would eventually be replaced by an anapsid skull, which is what we find in modern turtles."

Although the new study represents a major step towards understanding the reptile tree of life, Bever emphasizes that it will not be the final chapter in the science of turtle origins.

"The beauty of scientific discoveries is that they tend to reveal more questions than they answer" said Bever, "and there is still much we don't know about the origin of turtles. Which of the other diapsid groups form their closest cousin? What were the ecological conditions that led to the evolution of the turtle's shell and anapsid skull? And how much of the deep history of turtle evolution can be discovered by studying the genes and developmental pathway of modern turtles?"

G. S. Bever, Tyler R. Lyson, Daniel J. Field, Bhart-Anjan S. Bhullar. Evolutionary origin of the turtle skull. Nature, 2015; DOI: 10.1038/nature14900

Desmatochelys padillai, the oldest sea turtle

The skeleton of Desmatochelys padillai measures almost 2 meters.
Photo Credit:PaleoBios/Cadena

Scientists at the Senckenberg Research Institute in Frankfurt have described the world's oldest fossil sea turtle known to date. The fossilized reptile is at least 120 million years old -- which makes it about 25 million years older than the previously known oldest specimen. The almost completely preserved skeleton from the Cretaceous, with a length of nearly 2 meters, shows all of the characteristic traits of modern marine turtles. The study was published in the scientific journal PaleoBios.

"Santanachelys gaffneyi is the oldest known sea turtle" -- this sentence from the online encyclopedia Wikipedia is no longer up-to-date. "We described a fossil sea turtle from Colombia that is about 25 million years older," said Dr. Edwin Cadena, a scholar of the Alexander von Humboldt foundation at the Senckenberg Research Institute. Cadena made the unusual discovery together with his colleague from the US, J. Parham of California State University, Fullerton.

"The turtle described by us as Desmatochelys padillai sp. originates from Cretaceous sediments and is at least 120 million years old," says Cadena. Sea turtles descended from terrestrial and freshwater turtles that arose approximately 230 million years ago. During the Cretaceous period, they split into land and sea dwellers. Fossil evidence from this time period is very sparse, however, and the exact time of the split is difficult to verify. "This lends a special importance to every fossil discovery that can contribute to clarifying the phylogeny of the sea turtles," explains the turtle expert from Columbia.

The fossilized turtle shells and bones come from two sites near the community of Villa de Leyva in Colombia. The fossilized remains of the ancient reptiles were discovered and collected by hobby paleontologist Mary Luz Parra and her brothers Juan and Freddy Parra in the year 2007. Since then, they have been stored in the collections of the "Centro de Investigaciones Paleontológicas" in Villa Leyva and the "University of California Museum of Paleontology."

Cadena and his colleague examined the almost complete skeleton, four additional skulls and two partially preserved shells, and they placed the fossils in the turtle group Chelonioidea, based on various morphological characteristics. Turtles in this group dwell in tropical and subtropical oceans; among their representatives are the modern Hawksbill Turtle and the Green Sea Turtle of turtle soup fame.

"Based on the animals' morphology and the sediments they were found in, we are certain that we are indeed dealing with the oldest known fossil sea turtle," adds Cadena in summary.


Cadena, E.A. and J.F. Parham. Oldest known marine turtle? A new protostegid from the Lower Cretaceous of Colombia. PaleoBios, September 2015

Friday, September 4, 2015

The ancestral squamate was oviviparous ― I think

All members of the sand boa genus Eryx give birth to live young, except the 
Arabian Sand Boa, Eryx jayakari. This suggests that E. jayakari (left) 
re-evolved egg-laying from a viviparous ancestor. Right the viviparous Kenyan 
sand boa Eryx colubrinus.  Photo credits: Rick Staub and Arkive, and 
Roy Stockwell.
I very much dislike chicken and egg questions because it immediately sucks you into an argument with a creationist, most of whom simply don't get it. As Wright et al. (2015) point out the answer is clear from an evolutionary standpoint. The amniote egg, existed by the time the earliest amniotes (mammals and reptiles) diverged from one another about 325 million years ago, long before the first chicken (= birds) walked the Earth. Today, the majority of living amniotes are oviparous, including all birds, crocodylians, tuataras, turtles, and monotreme mammals. However, squamates are far more diverse in their approach to giving birth or laying eggs.
Approximately 20% of squamate species are viviparous, and this complex of traits has been estimated to evolve independently over 100 times across the squamate phylogeny. Viviparous species, developing embryos are retained in the mother's uterus for the entire duration of embryonic development. The traditional view of laying eggs or giving birth in amniotes is that the most recent common ancestor of squamates, which lived ~200 mya, was oviparous, as it inherited the same ancestral parity mode that characterizes all other reptiles.
The transition from oviparity to viviparity requires extensive modification of uterine physiology and morphology. For example, uterine shell glands in oviparous species secrete calcium during the discrete period of eggshell construction. In viviparous species, shell gland function has been modified to provide calcium to the embryo throughout gestation. True “ovoviviparity” does not exist in squamates, as all examined viviparous squamates have some form of placenta composed of both maternal and embryonic tissue.
The uterine structure of oviparous species is, therefore, modified into the maternal half of the placenta in viviparous species. The embryonic portion of the placenta is composed from the same extra-embryonic membranes that are present in all amniote eggs. Most squamate placentae are relatively simple structures used primarily for gas exchange and water transport, but a more elaborate placenta that facilitates significant nutrient exchange has evolved at least six times in squamates. Underlying the evolutionary transition to viviparity and a placenta are significant changes in gene expression of hundreds of genes.
In a new paper Wright et al. (2015) re-evaluate support for the provocative idea that the first squamates were viviparous. They test the sensitivity of the analysis to model assumptions and estimates of squamate phylogeny. They found that the models and methods used for parity mode reconstruction are highly sensitive to the specific estimate of phylogeny used, and that the point estimate of phylogeny used to suggest that viviparity is the root state of the squamate tree is far from an optimal phylogenetic solution.
The ancestral state reconstructions are also highly sensitive to model choice and specific values of model parameters. A method that is designed to account for biases in taxon sampling actually accentuates, rather than lessens, those biases with respect to ancestral state reconstructions. In contrast to recent conclusions from the same data set, Wright et al. (2015) found that ancestral state reconstruction analyses provide highly equivocal support for the number and direction of transitions between oviparity and viviparity in squamates. Moreover, the reconstructions of the ancestral parity state are highly dependent on the assumptions of each model. The authors conclude that the common ancestor of squamates was oviparous, and subsequent evolutionary transitions to viviparity were common, but reversals to oviparity were rare. The three putative reversals to oviparity with the strongest phylogenetic support occurred in the snakes Eryx jayakari and Lachesis, and the lizard, Liolaemus calchaqui. The authors emphasize that because the conclusions of ancestral state reconstruction studies are often highly sensitive to the methods and assumptions of analysis, researchers should carefully consider this sensitivity when evaluating alternative hypotheses of character-state evolution.


Wright AM, Lyons KM, Brandley MC, Hillis DM. 2015. Which came first: the lizard or the egg? Robustness in phylogenetic reconstruction of ancestral states. Journal of Experimental Zoology (Mol. Dev. Evol.) 324B:504–516.

Tuesday, September 1, 2015

When sister species live together, Tegu lizards in Argentina

Two Tegus, Salvator merianae and S. rufescens JCM
When two closely related species live side by side it is generally assumed that they have some way of dividing the resources so that they are not in direct competition with each other. The large terrestrial lizards the Black and White Tegu, Tupinambis (=Salavator) merianae, and the Red Tegu, T. (=Salvator) rufescens provide a model system to examine the role of life history factors in trophic niche divergence because they share several bioecological traits. They have similar body sizes and share external morphology and generalized foraging habits. Phylogenetic studies suggest the two species are sisters. In Argentina, they occur in parallel allopatric zones from approximately 10–40°S. Tupinambis rufescens occurs further west than T. merianae. However, they both occupy a large contact zone. These species differ in habitat requirements in allopatric areas, but in the contact zone the species use the same landscape and habitat resources. Moreover, T. merianae and T. rufescens select landscapes with a large proportion of forest and shrubs than the mean landscape availability in contact zones.

In a new paper López Juri et al. (2015) evaluate the trophic niche segregation between merianae and rufescens in a contact zone to understand how life history traits (body size, sexual body size dimorphism, sexual maturity and reproductive activity) might influence the feeding ecology of these lizards and lead to trophic niche differentiation between species. Their results suggest that, although both species are omnivorous, they exhibit a tendency to specialize, with arthropods being dominant in the diet of merianae and fruits and seeds being dominate in the diet of rufescens. The two species have broad trophic overlap, however, while both species share several prey items, the relative importance of each item varied between them. These differences may be important for niche segregation, mainly because the prey items considered fundamental were different between species, suggesting a differential use of certain resources. T. merianae is often associated with anthropogenic areas with cultural vegetation and remnant shrub lands where few vertebrate species remain which may explain the low diversity of food items and the dominance of arthropods and some rodents in the diet composition. Their results indicate that body size, sexual maturity and reproductive activity are relevant factors influencing the diet of these species. Life history traits of these two species of Tupinambis are important because they shape diet composition, contributing to interspecific segregation of the trophic niche and, therefore, allowing species coexistence.


López Juri G, Naretto S, Mateos AC, Chiaraviglio M, Cardozo G. 2015. Influence of life history traits on trophic niche segregation between two similar sympatric Tupinambis lizards. South American Journal of Herpetology, 10(2): 132–142.