Wednesday, January 28, 2015

Dwarf Boas

This post will soon become available in Spanish!
Este post pronto estará disponible en español!

Ambergris Cay Dwarf Boa (Tropidophis g. greenwayi)
Now that the USA and Cuba are finally warming up to one another after a chilly fifty years, we might be poised to learn a lot more about a really interesting group of snakes that reach their highest diversity on Cuba. These are the tropidophiids, or "dwarf boas". Their name is a little misleading—like the splitjaw snakes, they were once thought to be related to the true boas, and the name sticks even now that we now know better. At least the dwarf part is accurate: most tropidophiids are only 1–2 feet long. But this unassuming group of drab, nocturnal, live-bearing snakes holds more surprises and lessons about snake evolution that one would expect at first glance, with no shortage of interesting natural history to boot.

Top: Tropidophis melanurus constricts an anole
From Torres et al. 2014
Bottom: Madagascar Ground Boa
(Acrantophis madagascarensis)
constricts an oplurid lizard
Tropidophiids eat mostly frogs and lizards, and they constrict their prey in the same way as true boas: by winding the anterior part of their body neatly around their prey like a rope around a windlass, usually with an initial twist in the first loop, so that the snake's belly faces its head. This behavior, along with their relatively large gape size, seemed to suggest that they were related to the true boas (family Boidaesensu stricto), including well-known tree boas, boa constrictors, and anacondas. All true boas are neotropical and there are quite a few in the West Indies, so unlike many of the other boid "hangers-on" (such as the Malagasy Sanzinia & Acrantophis, African Calabaria, North American rosy and rubber boas, Pacific Candoia, and Old World sand boas), a close relationship between tropidophiids and boids was easy to accept in terms of the biogeography of the living species. A comparative analysis of constriction behavior in extant alethinophidian snakes done by Harry Greene and Gordon Burghardt showed that this pattern of constriction is shared by essentially all "henophidian" snakes, including booids, pythonoids, and some uropeltoids, notwithstanding a few fossorial species that have apparently secondarily lost constriction behavior alltogether, because it doesn't work in tight spaces.1

Top: Panamanian Dwarf Boa (Ungaliophis panamensis),
a member of the group to which tropidophiids were
once thought to be most closely related.
Bottom: Red Pipesnakes (Anilius scytale)
don't resemble tropidophiids very closely,
but we now think that they are each others'
closest living relatives.
In particular, what we now call tropidophiids were thought to be particularly closely related to two other small genera of neotropical boids, Exiliboa and Ungaliophis, which they superficially resemble both morphologically2 and ecologially. These still share their common name of "dwarf boa", but about 15 years ago a new picture began to emerge. While DNA from Exiliboa and Ungaliophis suggested that they were indeed related to true boas, evidence from both mitochondrial and nuclear DNA and immunological proteins of Tropidophis and Trachyboa, along with details of their muscular, circulatory, and reproductive anatomy, suggested that they were most closely related to the monotypic family Aniliidae, which contains a single South American species known as the Red Pipesnake (Anilius scytale). As far as we know, Anilius doesn't normally constrict its prey3, because it mostly forages underground on elongate vertebrates such as eels, caecilians, amphisbaenians, and other snakes, similar to various Asian pipesnakes to which it was once thought to be closely related. But, we are now fairly certain that these Asian pipesnakes are convergent with Anilius, that tropidophiids and aniliids are each others' closest relatives, and that the similarity between the gape size and constriction behavior of tropidophiids and that of boas and pythons probably still represents the shared retention of a paired morphology/action pattern used by their common ancestor, it's just a common ancestor that is much older than we originally thought. Estimates suggest that tropidophiids and aniliids diverged from one another 60-110 mya in South America4, after their common ancestors were isolated from those of all other modern alethinophidian snakes, which radiated in Africa following the mid-Cretaceous split-up of west Gondwana 70-120 mya. This was the split that formed South America and Africa, and we are now getting used to diving the alethinophidians into two major lineages, Amerophidia (tropidophiids and aniliids) and Afrophidia (everybody else), instead of into a monophyletic "crown-group" Macrostomata containing boas, pythons, and caenophidians, and a basal group of non-macrostomatan pipesnakes more similar in ecology to scolecophidians. My snake taxonomy article from 2013 is actually out-of-date with respect to this major shift in snake taxonomy, because at the time it was still unclear to me (and there are still some strong arguments from paleontologists that the molecular data may be misleading).

The Greater Antilles, Bahamas, and Turks & Caicos
The "new" family Tropidophiidae consists of two species of "eyelash dwarf boas" in the mainland genus Trachyboa (there we go with the boa thing again), and the diverse genus Tropidophis, which contains 32 species in total: 5 from mainland South America, and a West Indian radiation consisting of 17 Cuban species (one of which is shared with Jamaica and one with both Jamaica and Hispaniola), 1 on Hispaniola (shared with Cuba), 5 on Jamaica (two shared with Cuba), 2 in the Bahamas, one from the Turks & Caicos Islands, one each on the three Cayman Islands (Grand Cayman, Little Cayman, and Cayman Brac), and one endemic to Navassa Island, a small, uninhabited, disputed island in the Caribbean Sea between Cuba, Jamaica, and Hispaniola (which is known from four specimens and has not been seen in over 100 years). The West Indian species, particularly the Cuban ones, represent a radiation which rivals and parallels that of Darwin's finches. Morphological and molecular data suggest that the 17 species on Cuba are descended from a single colonization event, and that the island species appear to be more distantly related to the mainland ones than they are to Trachyboa, although four-fifths of the species of Tropidophis have no published sequence data yet so both of those conclusions could change.

Tropidophis xanthogaster bleeding from the mouth,
with blood behind the spectacle making the eyes appear red.
From Torres et al. 2013
As early explorers and biologists collected these snakes from bromeliads, within stone walls, and underneath rocks, they noted that species of Tropidophis made no effort to escape their collection, but rather coiled up into tight balls when captured. Another peculiar defensive behavior was soon noted—autohemorrhage of the nose and mouth. In other words, these snakes spontaneously bleed from these orifices and smear the blood all over themselves when handled. Creepily, the space between their spectacle and their eyes fills with blood momentarily beforehand, so that their eyes appear to flash red. Blood collected from their mouths doesn't clot for over half an hour, whereas blood collected simultaneously from their tails has clotted after 10 minutes, and the mouth blood is more acidic and has fewer red blood cells, presumably because it is mixed with saliva. However, it is not harmful to frogs or lizards, so it is not a substitute for venom. The exact function is unclear, but it appears to be to freak out would-be predators. Like many snakes, Tropidophis habituates to captivity and eventually does not exhibit this behavior.

Tropidophis melanurus, the largest species of Tropidophis
and the first described, from Cocteau & Bibron's 1843
volume on reptiles
in de la Sagra's Histoire physique, politique,
et naturelle de l’Ile de Cuba
Just when you thought things couldn't get any more interesting, brace yourself, because most Tropidophis can change color! They are light silver-white at night, when they are active, and dark grayish-brown during the day, when they are not. It takes a Tropidophis 1-2 hours to go from completely light to completely dark, which they accomplish via mobilization of melanosomes (organelles containing the light-absorbing pigment melanin) from the core of a melanophore cell deep within their skin into finger-like extensions of the melanophore that are closer to the surface of the skin, partially blocking stationary xanthophores and iridiophores, which contain yellow, blue, or green pigments. Both adults and juveniles undergo diel color change, and it does not seem to be affected by age, sex, pregnancy, or feeding, although prior to shedding snakes remain dark and inactive for several days. The change is probably predominantly triggered by photoperiod, but exposure to cool temperatures (<63°F) can elicit a partial change from dark to light even in the middle of the day. When captive snakes were transported from Cuba to Czechoslovakia, they became jet-lagged—it took them several days to synchronize their rhythm to the new photoperiod, and keeping them in complete darkness for several days desynchronized their rhythm from that of the sun. The proposed function of this color change is to help nocturnally-active snakes retain their body heat, as light-colored objects lose heat more slowly than dark-colored ones. This is probably similar to the reason that Round Island Splitjaw Snakes, Pacific Keel-scaled Boas (Candoia carinata), and the Hogg Island race of Boa constrictor also become lighter-colored at night.

Tropidophis pardalis on a Cuban stamp
There's much more to learn about tropidophiids, the Cuban radiation of Tropidophis in particular. To date, little ecological information has been collected on most species, owing in part to their rarity and in part to the difficulty of working in the region. How do five or six sympatric species partition resources and coexist in various parts of Cuba? What was the order of speciation and colonization of the islands, and when did it happen? Hopefully tropidophiids will be around long enough for us to find out. They are faced with numerous threats. As in many places, local people not especially fond of them, despite the fact that no Greater Antillean snakes are dangerous to people. Collection for the pet trade may also be a concern, particularly since one former government official in the Turks & Caicos Islands apparently granted a permit to reptile dealers to remove thousands of Tropidophis greenwayi from North Caicos for the pet trade, allegedly implying that it would be preferred if they removed all of the snakes! Throughout the West Indies, most native ecosystems have been absent for centuries, and increasingly rapid development, especially due to tourism, threatens what little remains. And introduction of non-native predators, particularly the Small Indian Mongoose (Herpestes javanicus), may be their biggest threat. As early as 1919, herpetologist Thomas Barbour wrote "In Jamaica [Tropidophis maculatus] is almost extinct owing to the appetite of the introduced mongoose". Ironically, Operation Mongoose was the codename for the Kennedy administration's attempt to create Cuban diplomatic, political, and economic isolation in hopes of weakening Castro’s regime. Cats, dogs, rats, goats, pigs, cane toads, and even other introduced snakes also threaten not just tropidophiids, but all 120+ snake species endemic to the West Indies as well as the rest of the native fauna. Improved PR and conservation programs have benefited several lizard species, and could help snakes too.

Tropidophis haetianus
I'm going to go ahead and wager that we'll discover a few new species of Tropidophis in the not-too-distant future, and that possibly the mainland species will get moved into a new genus. I also think that we need a more creative common name for them than "dwarf boa", preferably one that doesn't include the word "boa" at all. One existing option is "wood snakes", which is mediocre at best. They are also called "rock pythons" in the Caicos Islands, an equally misleading name as "dwarf boa", and "shame snakes" on Andros Island in the Bahamas, which may refer to their head-hiding defensive behavior. However, my favorite is the name they are known by in many parts of the West Indies: "thunder-snakes", because they are more frequently seen after severe rainstorms. Caribbean Thunder-snakes has a nice ring to it, and it could help improve their image.

1 1: Constriction behavior has become a lot more variable within the Colubroidea, where it has also been lost in several venomous lineages. Venom and constriction can be thought of as two different solutions to the same problem—how to kill large prey without exposing yourself to undue risk. Also, the contention that constriction and large gape size were lost in fossorial henophidians (aka "regressed" macrostomatans, including uropeltids, anomochilids, and aniliids) is seemingly contradicted by the complex multipinnate morphology of their jaw adductor muscles, which is sufficiently similar to that of their lizard ancestors that it is unlikely to have re-evolved in the exact same way multiple times. This problem might also be an issue for scolecophidians, given that they have similar jaw muscle morphology to pipesnakes but appear to be more closely related to other living snakes than they are to some basal fossil macrostomate snakes with limbs (symoliophiids). Stay tuned for more on the unresolved relationships at the base of the snake family tree, including a look at what fossil snakes can tell us.

2 2: All four genera (Exiliboa, Ungaliophis, Tropidophis, and Trachyboa) either completely lack a left lung or have a greatly reduced one, a characteristic they share with anomochilids and some caenophidians, but not with most other henophidians, which have a somewhat reduced but functional left lung. In addition, all four genera also have a "lung" on the dorsal wall of the trachea: the tracheal cartilages do not form closed rings but remain open on the top, where a greatly expanded ligament forms the tracheal lung. It has alveoli just like a regular lung, which are especially deep near the head, and is contiguous with the true lung in the vicinity of the heart. But, although this might seem like very strong evidence that these four genera are closely related, tracheal lungs of diverse structure are widespread among snakes, being found in certain scolecophidians, xenophidiids, acrochordids, vipers, atractaspidids, sea snakes, and many colubroid snakes.

3 3: A tantalizing bit of evidence emerged in 2008—biologists in Brazil videotaped the prey subjugation behavior of a captive Anilius scytale, which essentially constricted an amphisbaenian that they tried to feed it. In general its constriction behavior agreed with that of other henophidia, although it was more variable in the particulars, which could have been due to the difficulty of holding onto the elongate, "vigorous and constantly twisting prey". But, data from a single observation do not a generalization make, and more studies are needed.

4 4: Fossils of t
en extinct species in five genera from the Paleocene, Eocene, and Oligocene of Europe, Africa, & North and South America have been assigned to the Tropidophiidae, although all of them are probably actually either ungaliophiines or stem afrophidians. Two genera, Falseryx and Rottophis, both from the Oligocene of western Europe, have some similarities with living tropidophiids as well as with ungaliophiines, but for the most part their skulls are poorly preserved, leaving paleontologists to work on just their vertebrae. Paleogene erycines dominated the snake fauna of North America prior to the Miocene explosion of colubroids, but as far as we know all of these species were much more closely related to modern rosy and rubber boas than they were to tropidophiids. The only unequivocal tropidophiid fossils are from the Pleistocene of Florida and the Bahamas.


Thanks to Kenny Wray, Nick Garbutt, Alex Figueroa, Patrick Campbell, and Carlos De Soto Molinari for the use of their photographs.


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Hedges, S. B., A. Estrada, and L. Diaz. 1999. New snake (Tropidophis) from western Cuba. Copeia 1999:376-381 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Tuesday, December 16, 2014

What's the big deal about these snake genomes anyway?

This post will soon become available in Spanish

King Cobra (Ophiophagus hannah; top) and
Burmese Python (Python bivittatus; bottom),
the two snake species whose genomes
were fully sequenced in 2013
One year ago today, the first snake genomes ever sequenced hit the newsstands. OK, so two papers in Proceedings of the National Academy of Sciences isn't exactly the cover of Time magazine to most people, but it was big enough news that it was covered by The Huffington Post and the two most prominent interdisciplinary scientific journals, Science and Nature, the former devoting a special section to the event. One year later, dear reader, welcome to the Life is Short, but Snakes are Long coverage of the snake genome project. So just what is the big deal about these snake genomes anyway, and what's changed in snake biology in the year that they've been available?

In one way, sequencing a snake genome means that snakes finally join the illustrious ranks of lab animals like the mouse, rat, guinea pig, fruit fly, and amoeba, all of whom have already had their genomes sequenced. By now the genomes of several hundred species have been sequenced, starting with a virus in the 1970s, and the first archaeon, bacterium, and eukaryote within one year of one another in 1995-96. The first animal genome sequenced was that of the model nematode Caenorhabditis elegans in 1998, and the first vertebrate was a pufferfish, so chosen because its genome is so small, in 2002 (although an incomplete first draft of the human genome preceded that by a year). As of 2014, we're now up to just over 100 vertebrate species, about 60 of which have been annotated and formally published, as well as numerous other animals, plants, fungi, protists, and prokaryotes. Last week, Science highlighted drafts of 38 new bird and 3 new crocodilian genomes, the largest single release of vertebrate genomes to date. But we are still a long way from sequencing the genomes of all known species. Why have we chosen the species we have? What does it mean to sequence a genome, exactly, and why do we do it?

Breakdown of what the human genome
consists of. Exons are coding DNA.
From Reece et al. (2013)
We use the word genome to refer to all the DNA within a single organism. Confusingly, this is not quite the same thing as saying all the genes in an organism, because we usually only call sections of DNA "genes" if we know what they do. You've probably heard that 98% of the human genome is "junk", or non-coding, DNA, which is just another way of saying that we haven't figured out what it does yet. Actually, we now know lots of things that non-coding DNA is good for, but we still usually don't call most of that DNA "genes" because we use that word specifically to mean sections of DNA that are read out via RNA and translated (usually) into proteins, which then have obvious effects on cells and the body. Non-coding DNA can also have effects on the body, often by regulating other genes, but it works in a more complicated way that we don't yet fully understand, so we tend make over-generalizations about it or dismiss it as unimportant.

Avian tree of life based on whole-genome
sequences. We're still several years away from
a tree like this for squamate reptiles.
From Jarvis et al. 2014
When we say we have sequenced the genome of an organism, we mean that we have read the sequences of all of its DNA, every one of its genes and all of its non-coding DNA, even if we don't know what it all does. The -ome suffix is added to the word 'gene' to signify "all". Yogis will be familiar with the Sanskrit word Om, which means "the whole thing", something that encompasses the entire universe in its unlimitnedness. Other fields in biology that consider all constituents of something collectively have picked up on this neologism, so we have proteomics (the study of all the proteins in a particular organism), transcriptomics (the study of all the RNA), and so on. Genomes are huge1, and we've strategically chosen species to sequence that are scattered across the diversity of life so that we can construct a skeletal tree of life based on genomic data. We have high confidence in such a tree2 because whole genomes contain so much data that trees built from them are more likely to reflect true evolutionary relationships than trees built from just one or a few genes. So we've selected exemplars from each major group of organisms to start out with (e.g., one sea urchin, one sea squirt, one lamprey), and eventually we'll go back and fill in the gaps. By sequencing the King Cobra (Ophiophagus hannah) and Burmese Python (Python bivittatus) genomes first, we're setting these species up to become model organisms, exemplars, and in some ways stand-ins for all of snake diversity in many future studies.

Understanding the genes controlling variation among individuals
of the same species, like the color morphs of these Groundsnakes
(Sonora semiannulata), must await population genomics
and a better understanding of gene expression regulation
When we sequence a genome we read all the DNA from a single individual3. This is different from knowing all the possible variants (often called alleles) of those genes. It's often said that a person has "the genes for" something, when in reality all people have the same genes, with different alleles. For example, if the person whose genome was sequenced in the Human Genome Project had brown eyes, we'll just have the gene sequences for brown eyes, not for blue or green. In order to get an idea of all the possible variants of all the genes in a species, we'll need to sequence the genomes of many individuals. Some genes, such as those involved in the immune system, have over 1,500 alleles (the "gene pool"), no more than two of which occur within the genome of a single individual (one from the mother and one from the father). So understanding the entire gene pool of a species is a very daunting task, given that we only have whole genomes for a few hundred species (one individual each), with multiple individuals of a few species, including humans.4 Population genomics is an emerging field, yet to be applied to snakes in any form, although apparently a few projects are in the works.

So what have we learned from these snake genomes? Here are the basics:
  • Snake genomes are about half the size of the human genome (although an organism's complexity is not directly proportional to its genome size; for example, some salamander genomes are more than 60 times larger than the human genome).
  • The proportion of repetitive elements ("junk DNA") in snake genomes is about the same as that in humans (~60%).
  • Snakes have a faster baseline rate of evolution than other reptiles, birds, or mammals, as
    Red represents fast rates of neutral substitution
    From supplement to Castoe et al. 2013
    evidenced by their larger accumulation of neutral substitutions. and colubroid snakes have rates even faster than that of snakes at large.
  • Adaptive evolution (as evidenced by functional, non-neutral, changes to genes) in snakes has happened to over 500 genes, especially those involved in the development of the limbs, spine, skull, and eye, and those regulating the function of the cardiovascular system, lipid and protein metabolism, and cell birth and death. We already knew that all of these systems in snakes were highly modified relative to other vertebrates, and now we know that the genes that underlie them are too.
  • Some groups of genes have grown or shrank in snakes - for example, snakes have a lot more genes coding for vomeronasal receptors, and a lot fewer genes coding for opsins, which are light-sensitive proteins in the eye. This makes sense given what we know about snake sensory systems.
  • Changes to gene expression that happen after a snake feeds involve thousands of genes that control rapid changes in organ size - but genes that control cell division change in the kidney, liver, and spleen, organs that grow by cell division, but not in the heart, which grows when individual existing cells get larger.
  • Snake genomes contain endogenous viral elements from three families of viruses that have recurrently infiltrated their DNA over the past 50 million years. This is actually not rare, although it is bizarre and awesome that the 'fossils' of these ancient viral genomes can be identified in their host genomes even after tens of millions of years, and it can help us better understand both the biology of viruses and that of their snake hosts, including how viruses have contributed functions to the genetic repertoires of their hosts.
From the cobra genome in particular, we've learned or confirmed a great deal about the evolution of snake venoms. In particular, we now know that, unlike the venom of the platypus, the only other venomous vertebrate with a sequenced genome, snake venom has evolved primarily through gene duplication and restriction. Many venom proteins probably evolved like this:
  1. A snake has a gene that makes a protein somewhere in its body, including possibly in its salivary or venom gland5
  2. The gene for that protein is duplicated by accident during routine DNA replication or repair, resulting in a new, spare copy of the gene
  3. The effects of selection are relaxed on the duplicate gene, which gives it opportunities to mutate
  4. Mutations to transcription-factor binding sites change the signal for where the duplicate gene should be expressed, causing the new protein to be made only in the venom gland
  5. If the new protein helps the snake catch more prey, it improves fitness and causes natural selection
  6. Because the old protein is still being made, the new gene and protein are free to evolve to become more toxic or to take on some new function
  7. The new copy of the gene may become duplicated again, and subsequent new copies may mutate further, leading to diversification within a gene/toxin family6
The King Cobra venom gland, with
expression profiles of the venom (left) and
accessory gland (right). From Vonk et al. 2013
It's not yet clear to what extent the evolution of these novel toxic venom proteins corresponded with a shift to higher levels of their expression in the venom gland and lower levels of expression elsewhere. Although it seems obvious that their expression in non-venom-gland tissues would be harmful, their non-toxic orthologs are expressed in tissues as diverse as the kidney and brain in pythons, and no one has yet measured their expression outside of the venom gland in venomous snakes. Alternatively, gene duplication might have taken place after the change in function, if the genes in question were alternatively spliced to produce both toxic and non-toxic proteins from the same gene. Evolution  of siRNA and other regulatory elements (which is hard to detect because there's still a lot we don't understand about how it works) could then restrict expression of a particular splice variant to the venom gland, which could explain why we're seeing evidence that the venom protein genes themselves are often still expressed in other tissues even though they are capable of coding for highly toxic proteins that must be maintained in the venom gland in a competent but inactive state.

The cobra genome by itself does not answer these questions, even with help from that of the python. In order to fully understand the evolution of snake venoms (with major implications for public health, particularly in developing countries, not to mention the potential of venoms to be used as drugs), we'll need genomic, transcriptomic, and proteomic data from numerous snake species.

Characterization of genomic biodiversity has the potential to change our understanding of evolution in fundamental ways. From explaining how snakes are capable of physiological feats to helping us understand how new genes appearwhat "junk DNA" does, and what the tree of life looks like, genome sequencing is one of the most exciting current frontiers in biology. As in many things, snakes are (one of) the last groups of vertebrates to the party (although it's worth noting that there aren't any fully annotated salamander or caecilian genomes yet). A snake genome doesn't add a whole lot to the picture of the vertebrate tree of life, because the Green Anole genome, sequenced in 2011, represents squamates on the tree, and no one is arguing that snakes aren't squamates. But, within squamates there are a number of puzzling unresolved relationships, including such fundamental questions as the origin of snakes and the placement of iguanians. In the interest of helping to shed light on these, and on the aforementioned complexity of snake venom evolution, another 10 or so snake genomes are likely to come out within the next couple of years, including those of the:
  • Texas Blindsnake (Rena dulcis)
  • Reticulate Wormsnake (Amerotyphlops reticulatus)
  • Red Pipesnake (Anilius scytale)
  • Mexican Burrowing Python (Loxocemus bicolor)
  • Round Island Splitjaw Snake (or "boa"; Casarea dussumieri)
  • Boa Constrictor (Boa constrictor)
  • Western Diamond-backed Rattlesnake (Crotalus atrox)
  • Speckled Rattlesnake (Crotalus mitchelli)
  • Copperhead (Agkistrodon contortrix)
  • Eastern Coralsnake (Micrurus fulvius)
  • Cloudy Snail-eating Snake (Sibon nebulatus)
  • Common Gartersnake (Thamnophis sirtalis)
As you can probably see if you know your snake taxonomy, these species represent a scattering of well-known snakes from each of the major branches of the snake tree. They have been strategically chosen to enable snake biologists to use them to put together a well-supported skeleton of the snake tree of life. However, several branches (such as the dwarf pipesnakes, acrochordids, and lamprophiids) are still missing.7 In particular, an atractaspidid genome would be useful in building a better understanding of the role of convergence in snake venom evolution - resolving the debate between proponents of a single ancient origin for venom and those of several more recent, independent origins. Genomes of scolecophidian blindsnakes and toxicoferan lizards such as Gila monsters will also help resolve this question. Hopefully, these genomes and others will continue to illuminate evolutionary biology for us in ways Darwin could have scarcely imagined.

1 Because genome sequences contain so much data, they are stored electronically and require a large amount of computing power and storage capacity. The computing power is actually more limiting than the biochemistry right now. A human genome contains about 6 billion base pairs (one for each person on Earth in 1999), which take up a couple of gigabytes. If that doesn't sound that impressive, imagine all that information stored 
in every one of your cells, then compare the size of a cell with that of a microchip here.

2 This is not to say that (as has been presumed by many) molecular data are inherently superior to morphological data, especially in the case of extinct fossil taxa, from which we cannot garner much molecular information (although that generalization too has been challenged).

3 How are the individuals whose genomes are sequenced chosen? The unsatisfying answer is that the scientists involved typically use whatever individuals are convenient. Specifically, the cobra and python genomes seem to have been taken from animals from the pet trade. We may not know the true geographic origin of these individuals, or even whether they might be the offspring of animals from two or more different parts of the species' range. Why is this important? If we sequence the genome of a cobra from Indonesia, but cobras in India have evolved different venom genes because of different evolutionary pressures, then we won't know that until we get some cobras from India. Taxonomic conclusions drawn from 
Boa constrictor gene sequences on GenBank are dubious because of the ambiguous origins of many of these specimensThe primary reasons to sequence a whole genome are subtly different from the reasons to sequence individual genes, and scientists doing these tasks have different questions. But, we should be cautious about inferring too much from the genome sequence of a single individual of any species.

4 Right now if you're a human you can actually get your whole genome sequenced for less than $5000, even though the first human genome cost over $3 billion, because we've optimized the process.

5 It's unclear how many venom proteins were originally made in the venom gland before they became toxic, and how many were recruited to this tissue following duplication. The original cobra genome paper by Vonk et al. implies that the latter is most common, whereas subsequent work by Hargreaves et al. uses gene expression data from Leopard Gecko salivary glands
 to suggest the former. Reyes-Velasco et al. used the python genome and transcriptome to suggest that venom genes are recruited preferentially from genes that are expressed at low levels in most tissues but at more variable levels than average across tissues.

6 Of the approximately 24 gene families that code for snake venom proteins, those that produce toxins that are known to be important in prey capture (e.g., the three-finger neurotoxins) have undergone repeated duplication and selection, whereas venom components that perform ancillary functions, such as helping the snake to relocate its bitten prey, do not show high rates of duplication or selection. These rates are probably further influenced by the need to target diverse receptors in different types of prey (in snakes with broad diets), and by predator-prey co-evolutionary arms races (in snakes with narrow diets).

7 A recent effort by a different research group generated a tree for Caenophidia using 333 loci totaling 225,140 base pairs for each of 31 snake species, almost 80,000 of which were informative. This is a drastic improvement on the 10 loci and maximum of 5,814 base pairs of the most comprehensive previous studies, but it is still a long way from the entire genome. Incredibly, they were still unable to resolve certain difficult parts of the snake family tree.


Thanks to JD Willson, Baloch Imrankhan, and Alison Davis Rabosky for the use of their photographs, and to Alison Davis Rabosky and Todd Castoe for providing me with information regarding genomics.


Alföldi et al. 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587-591 <link>

Armengaud, J., J. Trapp, O. Pible, O. Geffard, A. Chaumot, and E. M. Hartmann. 2014. Non-model organisms, a species endangered by proteogenomics. Journal of Proteomics 105:5-18 <link>

Castoe et al. 2013. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proceedings of the National Academy of Sciences 110:20645–20650 <link>

Cox, C. L. and A. R. D. Rabosky. 2013. Spatial and Temporal Drivers of Phenotypic Diversity in Polymorphic Snakes. The American Naturalist DOI: 10.1086/670988 <link>

Gauthier, J. A., M. Kearney, J. A. Maisano, O. Rieppel, and A. D. B. Behlke. 2012. Assembling the squamate Tree of Life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History 53:3-308 <link>

Hargreaves, A. D., M. T. Swain, M. J. Hegarty, D. W. Logan, and J. F. Mulley. 2014. Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biology & Evolution 6:2088-2095 <link>

Hargreaves, A. D., M. T. Swain, D. W. Logan, and J. F. Mulley. 2014. Testing the Toxicofera: Comparative transcriptomics casts doubt on the single, early evolution of the reptile venom system. Toxicon. DOI:10.1016/j.toxicon.2014.10.004 <link>

Jarvis et al. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320-1331 <link>

Losos, J., D. M. Hillis, and H. W. Greene. 2012. Who speaks with a forked tongue? Science 338:1428-1429 <link>

Mackessy, S. P. and L. M. Baxter. 2006. Bioweapons synthesis and storage: The venom gland of front-fanged snakes. Zoologischer Anzeiger 245:147-159 <link>

Pyron, R. A., C. R. Hendry, V. M. Chou, E. M. Lemmon, A. R. Lemmon, and F. T. Burbrink. 2014. Effectiveness of phylogenomic data and coalescent species-tree methods for resolving difficult nodes in the phylogeny of advanced snakes (Serpentes: Caenophidia). Mol. Phylogenet. Evol. 81:221-231 <link>

Reyes-Velasco, J., D. C. Card, A. Andrew, K. J. Shaney, R. H. Adams, D. R. Schield, N. R. Casewell, S. P. Mackessy, and T. A. Castoe. 2014. Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Molecular Biology and Evolution <link>

Schweitzer, M. H. 2011. Soft tissue preservation in terrestrial Mesozoic vertebrates. Annual Review of Earth and Planetary Sciences 39:187-216 <link>

Vonk et al. 2013. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proceedings of the National Academy of Sciences 110:20651–20656 <link>

Yadav, S. P. 2007. The wholeness in suffix -omics, -omes, and the Word Om. Journal of Biomolecular Techniques 18:277 <link>

Zelanis, A. and A. Keiji Tashima. 2014. Unraveling snake venom complexity with ‘omics’ approaches: challenges and perspectives. Toxicon <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Tuesday, November 25, 2014

The 9,999th Reptile

This post will soon become available in Spanish

Number of new snake species by decade, with highlights
Data from The Reptile Database
Linnaeus's 1758 Systema Naturae, the starting point of zoological nomenclature, described 118 species of reptiles, including 74 snakes (not counting the limbless lizards and amphibians he included in the same group). It took over 100 years for the number of described species of snakes to reach 1000, an event that probably passed without much notice amid the American Civil War. Since that time, new snake species descriptions have been added at the rate of about 15 a year, although molecular taxonomy has increased this pace over the last few decades. The trends for snakes and for reptiles as a whole have been similar, and on July 9th, 2014, a team of American, German, Lao, and Vietnamese scientists described a new species of gecko from Laos, which the journal Herpetological Review reported as the 10,000th reptile species. Needless to say, I was excited, but I was also extremely disappointed because I had been so hoping that it would be a snake! Rather than admit defeat and scrap this planned post, I emailed Peter Uetz at The Reptile Database, an incredible resource that I've praised before, to confirm that this gecko was indeed #10,000. As usual for taxonomy and as I should have suspected, the reality was a bit more complicated.

Although Cyrtodactylus vilaphongi was the 10,000th reptile species for a while, the order and position of entries in The Reptile Database is constantly changing. Although new species get added to the end of the list, it's common for two or more existing species to get synonymized or merged, which moves the position of all subsequent species up. Furthermore, sometimes species that were described long ago and subsequently synonymized are revalidated, leading to 'new' species that aren't really new in the sense that they have existed before. Finally, often existing species get split up, leading to additions that aren't as dramatic as legitimate new discoveries. This last complication is on the rise now that molecular systematics has enabled us to describe the cryptic diversity of some lineages, which are not all that morphologically distinct but may contain considerable genetic diversity.

At the time of my email to Peter last month, C. vilaphongi was the 9988th species, and (happily), a new snake, Siphlophis ayauma, was #10,000. Although this has probably changed again by now, I'm going to operate under the assumption that, since we can't really say with certainty that any particular species was #10,000, if it was a snake, it was probably one of the 11 brand new snake species that have been described so far this year. You can read about many of these on the blog 'Species New to Science', but I'm going to highlight them in a little more detail here.

Rhabdophis guangdongensis
From Zhu et al. 2014
The first new snake described this year, Rhabdophis guangdongensis, was collected by a team of Chinese herpetologists in Guangdong Province in 2008. The reason it wasn't described until the February 20th issue of the journal Zootaxa is because, as is often the case, it takes a couple of years to compare both the anatomy and the DNA of a suspected new species to reference specimens of known similar species and establish that the species really is new. In the past, particularly prior to the internet, the difficulty of doing this was a huge problem, resulting in close to half of all 'new' species later being invalidated as duplicates. The genus Rhabdophis  is distributed in southern and eastern Asia, and this is the 21st species. It's an extremely interesting genus from a chemical ecology perspective, because at least one species sequesters defensive chemicals from its prey and provisions them to its young (which I wrote about for Scientific American shortly after I started this blog). A recent paper by Yosuke Kojima and Akira Mori on the Japanese species R. tigrinus showed that females periodically leave wetlands for forest streams where they forage on toads, likely to obtain the necessary toxins for provisioning their offspring. The new species also has specialized structures, known as nuchal glands, on the back of its neck, so presumably it stores bufotoxins there as well, although this has yet to be verified.

Opisthotropis durandi
From Teynié et al. 2014
On March 3rd, a team of French, German, and Vietnamese scientists published a description of Opisthotropis durandi, a highly aquatic snake collected from the base of a waterfall in northern Laos. This is the seventh species of Opisthotropis described in the past 20 years, and the first from Laos (although other species are likely to occur there based on their occurrence in surrounding countries). Like the new Rhabdophis, it is also the 21st species in its genus. It is important to realize that, like most species new to science, this snake was already known by local people. It is called Ngou Koung or Ngou Kung, meaning “shrimp snake”, suggesting that it may eat shrimp. The pools at the base of the waterfall where the first specimen was found contained many small shrimp.

Eutrachelophis bassleri and its weird penis
From Myers & McDowell 2014
Harvey Bassler, a petroleum geologist, explored many of the Amazon's upper tributaries for his work during the 1920s and 30s, during which time he collected over 4,200 snakes on the side. Bassler deposited his magnificent collection in the American Museum of Natural History in 1934, and on March 6th this year Charles Myers and Samuel McDowell published a monograph in the Bulletin of the American Museum of Natural History describing a species of snake collected by Bassler in 1927, for which they erected a new genus, Eutrachelophis (‘beautiful-necked snakes’’). They also placed in this genus a species originally described by Boulenger in 1905, Rhadinaea steinbachi, which they renamed Eutrachelophis steinbachi. Although the two species (and a third, yet undescribed) have very similar skeletons, muscles, glands, viscera, and markings, they probably would have been placed in separate genera had they been described in the 19th or early 20th century because their hemipenes are so different. E. steinbachi has long but relatively normal-looking hemipenes, whereas E. bassleri  has extremely unusual heimpenes tipped with a dome-like structure so strange (at least within the world of snake hemipenes) that the authors wrote "we have seen nothing quite like [it]." Hemipenes were traditionally considered one of the most taxonomically-important structures in snakes1 because they were considered to be evolutionarily neutral (that is, unlikely to change in response to selection), but a growing awareness that evolution by both natural and especially sexual selection can influence the morphology of male genitalia led these authors to recognize that these two snakes were in fact close relatives. Although we await molecular confirmation, the authors propose a mechanism by which differential expression of Hox genes2 could cause such a rapid divergence in hemipenal morphology between two sister species.

Siphlophis ayauma
From Sheehy et al. 2014
On January 12th, 2008, a group of American and Ecuadorian herpetologists stopped for lunch at a grilled-chicken restaurant in Paute, Azuay province, Ecuador. They noticed a peculiar sun-faded snake on display in a jar of alcohol that they couldn't quite put a name to. Following negotiation with the restaurant owner, the specimen was acquired and determined to belong to the genus Siphlophis, but could not be identified to any known species. A few months later, another specimen was found alive about 100 miles to the north, and two more were discovered in 2011 about the same distance to the south. A fifth individual is now recognized to have been hiding out unnoticed in the collection of the Museo de Zoología, Pontificia Universidad Católica del Ecuador. Because of its red-banded head and its occurrence in the mountains near cold (achachay) streams, the new species was named Siphlophis ayauma after the Kichwa spirit Aya Uma, a good spirit devil who derives strength from nature, particularly from cold mountain pacchas (cascades) and is represented in Kichwa folklore as having a colorful red-banded head. This is the seventh species in the genus, the third species known from Ecuador, and the first new species of Siphlophis since 1940. The results are published in the April 1st issue of the South American Journal of Herpetology.

Philodryas amaru
From Zaher et al. 2014
In a montane grassland high in the Andes Mountains of southern Ecuador, another genus gained its 21st species this year: Philodryas amaru. Known to the Ecuadorian and Brazilian authors since 2005, a small population of these striped racers was formally described in Zootaxa on April 4th this year. The new species resembles Philodryas simonsii in color pattern, but differs noticeably in its hemipenis morphology. "Amaru" means "snake" in Kichwa, and is also the name of a snake deity who influences water and the economy. This diurnal snake lays clutches of 9-13 eggs underground in galleries and under decaying logs, and probably eats frogs and lizards. It is a close relative of the Galapagos racers that I've written about before.

Causus rasmusseni
From Broadley 2014; photo by Paul L. Lloyd
Night adders (genus Causus) are a small and unusual group of vipers found in sub-Saharan Africa. They were once thought to be the most primitive vipers and were placed in their own subfamily, but they are now grouped with the viperines even though they have a plethora of unusual features: platelike head scales, round pupils, a different hinge mechanism for their erectile fangs, incomplete fang canal closure, and elongate venom glands in most species. On April 25th of this year, Don Broadley3 described the first new species of Causus since 1905. He named it Causus rasmusseni after the late Jens Rasmussen, a Dutch expert on African snakes who died in 2005. This species is found only in the watershed between the Congo and Zambezi basins, where it co-occurs with three other species of Causus. Broadley first became aware that there might be a new species of night adder in this region in 1991, when he noticed pale gray C. rhombetaus from northwestern Zambia with black markings and low ventral scale counts. In 2013, someone sent him a picture of one eating a toad (another unusual adaptation that night adders share with several other snakes), which prompted him to look again at the unusual specimens and describe them as a new species. Few molecular data are available for Causus, so this diagnosis is based on morphology alone.

Micrurus potyguaraFrom Pires et al. 2014
Brazil is graced with nearly 400 species of snakes, including 30 of the world's ~80 species of coralsnakes. The morphology of coralsnakes is highly variable, and there are many misidentified specimens in museum collections, so it is often difficult to recognize new species. A group of Brazilian herpetologists working on the tri-colored coralsnakes from the endangered northeastern coastal forests discovered a new species, which they described in the June 5th issue of Zootaxa (if any of these dates are your birthday, then you share a birthday with that of a new species of snake!).

Top: Jaw of Lycodon aulicus
From Jackson & Fritts 2004
Middle: Lycodon zoosvictoriae
From Neang et al. 2014
Bottom: Lycodon cavernicolus
From Grismer et al. 2014
Wolfsnakes (genus Lycodon) are named for their fearsome-looking fang-like anterior maxillary teeth. Unlike the true fangs of vipers, elapids, and atractaspidids, wolfsnake teeth are not grooved or hollow and they have no venom. Instead, their strongly arched upper jaw helps them feed on skinks, whose hard, cylindrical bodies fit snugly into their diastema, or the gap between their anterior and posterior teeth. The wolf-like anterior teeth keep the skink from being squeezed out of the mouth, while the posterior teeth slice through the skink's cycloid scales. At least 16 of the nearly 60 species of Lycodon have been described since the 1990s, including two this June: Lycodon zoosvictoriae from the Cardamom Mountains of southwestern Cambodia, and L. cavernicolus from a limestone cave in peninsular Malaysia. The latter is a cave-adapted species, both specimens of which were found climbing several feet above the cave floor, in total darkness. It's likely that they eat a cave-adapted gecko. Many of the caves in this region are in immediate danger of being quarried for cement before their endemic fauna and flora can be fully documented. Both of these species were also described in Zootaxa, which is a relatively new journal dedicated almost exclusively to rapid publication of new species descriptions, with the stated goal of aiding conservation efforts by circumventing the lengthy delays normally associated with publication of new science. Since its inception in 2001, Zootaxa has become a daily journal that has published nearly one quarter of all new animal taxa and nomenclatural acts in the last five years, including over 400 new species of reptiles and the 7000th species of amphibian.

"Cloudogram" of Crotalus triseriatus species group
showing the new nine-species arrangement
From Bryson et al. 2014
Just three days before the new gecko, a team of scientists from Mexico, the USA, and Canada published a genetic analysis of the Crotalus triseriatus species group, which contains small montane rattlesnakes found in Mexico and the southwestern USA. Although five species were historically recognized within the group, an analysis of seven nuclear genes revealed that there are at least nine species, including two that were previously recognized as subspecies and two more that have not heretofore been formally recognized. The paper described the two new species: Crotalus tlaloci, named for Tláloc, the Aztec god of rain, and Crotalus campbelli, named for herpetologist Jonathan Campbell. The authors of this paper suggest that these rattlesnakes speciated rapidly from a single common ancestor during the uplifting of the Trans-Mexican Volcanic Belt near the end of the Neogene period 2.6 million years ago, which makes sense because they are not very mobile and populations of their common ancestor likely would have become isolated from one another  on various "Sky Islands" of suitable habitat during the genesis of this new mountain range. Many species are endemic to the high-altitude pine-oak forests and grasslands of this region, which has become famous as the overwintering grounds of the Monarch Butterfly.

Chironius diamantina
From Fernandes & Hamdan 2014
Surprise! Just when you thought we were through, at press time the description of four more new species of snake had just been published, all from relatively recent issues of Zootaxa. One is a Brazilian species of Chironius, one of my favorite genera. Chironius diamantina is the 16th species in the genus, which is unusual is having a very low, even number of dorsal scale rows (10 or 12), the central pair of which are strongly keeled, giving the snake a distinctly flat-backed appearance. This species is found in riparian forests along rocky streams in coastal Brazil, not too far south of the new coralsnake (above). Chironius are diurnal and generally eat birds and mammals. Another is a new Asian keelbackHerpetoreas burbrinki, from near the border of China, India, and Burma. which is relatively closely related to the Rhabdophis above. Finally, two new species from the large ground-dwelling Latin American genus Atractus, both small and described from single specimens collected decades ago in Colombia (perhaps they will one day be rediscovered). More new species from both of these groups will likely follow, given the taxonomic untidiness of their genera. [Update: shortly after publication David Salazar-Valenzuela alerted me to the fact that I had missed his description, with colleagues, of a third new Atractus from the cloud forests of northern Ecuador earlier this year, in the journal Herpetologica. They mention that some of the specimens were collected from under logs alongside an undescribed species of slender blindsnake of the genus Trilepida, so it seems we are at 3,500 this year without a doubt!] [[Update II: It seems I missed more than I thought - a new species of Trimeresurus from Sumatra was described in September from specimens collected in 1899, and a new Ninia from Trinidad was described in August from a 1988 specimen.]]

In addition to these 15 species, there are a couple of species of snake which were described long ago but that were revalidated recently, including several scolecophidians (Typhlops silus, first described in 1959; Afrotyphlops angeli, first described in 1952; and Letheobia acutirostrata, first described in 1916) and a rattlesnake (Crotalus armstrongi, originally described as a subspecies in 1979 and elevated by the same group that described C. tlaloci and C. campbelli). These are typically announced with less fanfare than the truly new descriptions that I've highlighted above.

Although it's actually been the slowest year for new snakes since 19974, we have 15 new snakes this year, bringing snakes to a total of 3,499 (and 2014 isn't over yet!). We could make it to 3,500 snakes in the same year that we hit 10,000 reptiles. I think these milestones in taxonomy emphasize the importance of reptiles and how much we have left to learn about them. I doubt that the pace of new species descriptions will slow down anytime soon, as experts estimate that less than 15% of the species on Earth have yet been described. Increasingly, reptiles, and snakes in particular, are becoming poster-children for biodiversity and conservation, a welcome change from their history of being overlooked and maligned. Soon, we will have high-quality global range maps for all species of reptiles, an achievement reached some time ago by amphibians, mammals, and birds, which will enable their incorporation into global assessments of vertebrate diversity and conservation planning. It's an exciting time.


Thanks to Peter Uetz at The Reptile Database for sharing with me some inside information, and to the authors of these papers for their photos.


Newspaper clipping from 10 January 1960
showing Broadley with his amputated finger.
You can see more at the finger's Facebook page
or listen to Broadley describe the experience here.
Angarita-Sierra, T. 2014. Hemipenial Morphology in the Semifossorial Snakes of the Genus Ninia and a New Species from Trinidad, West Indies (Serpentes: Dipsadidae). South American Journal of Herpetology 9:114-130 <link>

Broadley, D. G. 2014. A new species of Causus Lichtenstein from the Congo/Zambezi watershed in north-western Zambia (Reptilia: Squamata: Viperidae). Arnoldia Zimbabwe 10:341-350 <link>

Bryson, R. J., C. W. Linkem, M. E. Dorcas, A. Lathrop, J. M. Jones, J. Alvarado-Diaz, C. I. Grunwald, and R. W. Murphy. 2014. Multilocus species delimitation in the Crotalus triseriatus species group (Serpentes: Viperidae: Crotalinae), with the description of two new species. Zootaxa 3826:475-496 <link>

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Trimeresurus gunaleni
From Vogel et al 2014

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Atractus savagei
From Salazar-Valenzuela et al. 2014
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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.