Virgin Birth, the Color of Fossil Snakes, and More Recent Updates

This post will soon be available in Spanish

As I did in March, I wanted to highlight some recent and exciting updates to some of my older articles.

Snakes That Give Virgin Birth

Phylogenetic pattern of parthenogenesis in snakes
Molecular tree on left, morphological tree on right
From Booth & Schuett 2016

When I wrote about asexual reproduction in snakes in February 2014, new records of this phenomenon were rapidly accumulating, from snakes as distantly related as cottonmouths and boa constrictors. In a new paper, Warren Booth and Gordon Schuett review the knowns and unknowns of "virgin birth" in snakes, a subject which has become their specialty (it even has its own Facebook group). Although obligate parthenogenesis is still known only from Brahminy Blindsnakes (Indotyphlops braminus), the new summary reports that facultative parthenogenesis has now been documented in 20 species of alethinophidian¹ snakes, and this list is anticipated to grow, although so far confirmed cases are limited to five lineages: boids, pythonids, Acrochordus, Crotalinae, and Natricinae. This new synthesis formalizes one of the trends that I wrote about in 2014, namely distinguishing between "Type A" facultative parthenogenesis, in which the offspring produced are large clutches of viable females that seem to have a strange "WW" sex chromosome arrangement (apparently typical of boas and pythons), and "Type B" facultative parthenogenesis, which is where all the offspring are male and few are born alive, many with extreme developmental abnormalities (apparently typical of colubroids).

Most intriguing is the hypothesis laid out for explaining this dichotomy: that boas and pythons (and possibly other basal alethinophidian snakes) might have an XY sex determination system rather than a ZW one like most snakes. Changes from ZW to XY or vice versa (and between genetic and temperature-dependent sex determination) have been documented in geckos and turtles, and could have been overlooked in boas and pythons due to their similar-looking sex chromosomes (tests are currently underway to falsify or verify this hypothesis). If true, this would explain the production of all-female offspring by facultative parthenogenesis; instead of WW, those females would be XX, just like humans!

Identifying Snake Sheds

True-color representation of the fossil snake
(MNCN 66503) in McNamara et al. 2016.
The dentition looks too solenoglyphous for a
colubrid, although the 10-million year old specimen,
which is missing its head, has not and
probably can not be identified to species.

Ever since the first reports of color from the skin and feathers of dinosaur fossils were published in Science in 2010, I've been fascinated by the ability of paleontologists to see in color when they look into the past. A new paper in the journal Current Biology reveals the color of a fossil snake, determined from using scanning electron microscopy (SEM) to examine microfossils of certain types of skin cells, called chromatophores. So far, only melanin-based chromatophores (melanosomes, which are responsible for brown and black color) have been detected in fossilized skin and feathers, probably because they are the most resistant to the decomposition process. But, this study was also able to detect and measure other types of chromatophores from fossilized skin, including xanthophores (responsible for yellow, orange, or red color, derived from carotenoids or pteridines) and iridophores (responsible for iridescence). By comparing the fossil's chromatophore abundance and position to that of living reptiles, they were able to reconstruct the original color and pattern of the fossil snake's skin. For example, in the skin of living snakes, xanthophores with many more pteridine granules than carotenoid granules produce a red hue, whereas xanthophores with equal amounts of carotenoid granules and pteridine granules—as in the fossil—produce yellowish hues. Skin regions with abundant iridophores and xanthophores, but relatively few melanophores, are associated with green hues in some living skinks, whereas skin regions with many melanophores, a few xanthophores, and no iridophores suggest correspond to dark brown or black tones. As you can see in the depiction, this snake seems to have had a pale, creamy venter and a green back and sides, with areas of brown/black and yellow/green, perhaps not unlike modern Green Watersnakes (Nerodia floridana) or Boomslangs (Dispholidus typus).

Snakes Flying Without Planes

Photo and diagram of courtship behavior of Chrysopelea paradisi
Taken at the Sepilok Jungle Resort in Sabah, Malaysia
Female shown in gray, males in blue, green, and orange
From Kaiser et al. 2016

A new report on the mating behavior of Paradise Flying Snakes (Chrysopelea paradisi) showed that their courtship can involve multiple males. Although several experiments have been performed on the gliding behavior of these snakes, almost nothing is known about their natural history in the wild. Males of many species of snakes court females en masse by rubbing their chins along their bodies, a behavior which allows them to sense her sex pheromones and jockey for position. The role played by the female in choosing a male is unclear in most snake species; although conventional biological wisdom suggests that females should be the choosy sex, male-male competition seems to dominate courtship behavior in several species of snakes. Multi-male courtship behavior precedes mating in some well-studied temperate snakes (e.g., gartersnakes emerging from hibernation), as well as in some tropical species (e.g., anacondas, some other southeast Asian colubrids, such as Boiga irregularis and Dryophiops rubescens). Of course, it seems that most female snakes can store sperm for long periods of time, and they may have some control over which male's sperm to use to fertilize their eggs, so the genetic contribution of a female snake's male partners may not follow from their courtship or mating success. Unlike the terrestrial or aquatic mating balls documented for other snakes, the flyingsnakes in this observation were able to move as a unit for almost 50 feet through complex habitat—under a porch, up a tree—an adaptation that seems to fit their active, arboreal lifestyle and might help reduce the likelihood of a predatory attack during what must otherwise be a vulnerable time.

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1 In a few places, the authors use "alethinophidian" to refer to boas, pythons, and their relatives but not caenophidians, when instead they should have either used "henophidian" or "basal alethinophidian" (they mostly use the latter term throughout). Many people don't like the term "henophidian" because it is a paraphyletic group, but it is a convenient way to refer to non-scolecophidian, non-caenophidian snakes. In my mind it's essentially synonymous with "basal/stem alethinophidian". Alethinophidians are all snakes except for blindsnakes (scolecophidians), and Caenophidia is a subset of Alethinophidia. There are also at least three references to "Caenophidia + Colubroidea", which is confusing because Colubroidea is a subgroup of Caenophidia, and Caenophidia = Colubroidea + Acrochordus, which is perhaps what they meant.^↩

ACKNOWLEDGMENTS

Thanks to Gordon Schuett for clearing up some of the details of his recent paper.

REFERENCES

Booth W, Schuett GW (2016) The emerging phylogenetic pattern of parthenogenesis in snakes. Biological Journal of the Linnaean Society 118:172-186 <link>

Gamble, T., J. Coryell, T. Ezaz, J. Lynch, D. Scantlebury, and D. Zarkower. 2015. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Molecular Biology and Evolution 32:1296-1309 <link>

Kaiser H, Lim J, Worth H, O’Shea M (2016) Tangled skeins: a first report of non-captive mating behavior in the Southeast Asian Paradise Flying Snake (Reptilia: Squamata: Colubridae: Chrysopelea paradisi). Journal of Threatened Taxa 8:8488–8494 <link>

Kuriyama, T., K. Miyaji, M. Sugimoto, and M. Hasegawa. 2006. Ultrastructure of the Dermal Chromatophores in a Lizard (Scincidae: Plestiodon latiscutatus) with Conspicuous Body and Tail Coloration. Zoological Science 23:793-799 <link>

Li, Q., K. Q. Gao, J. Vinther, M. D. Shawkey, J. A. Clarke, L. D’Alba, Q. Meng, D. E. G. Briggs, and R. O. Prum. 2010. Plumage color patterns of an extinct dinosaur. Science 327:1369 <link>

McNamara, Maria E., Patrick J. Orr, Stuart L. Kearns, L. Alcalá, P. Anadón, and E. Peñalver. 2016. Reconstructing Carotenoid-Based and Structural Coloration in Fossil Skin. Current Biology <link>

McNamara, M. E., D. E. G. Briggs, P. J. Orr, D. J. Field, and Z. Wang. 2013. Experimental maturation of feathers: implications for reconstructions of fossil feather colour. Biology Letters 9 <link>

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

Snakes flying without planes

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By now, all of us herpetologists have heard quite enough 'Snakes on a Plane' jokes, thank you very much (they're second only to jokes about how we probably study STDs - never heard that one before). Meanwhile, in reality, snakes have been flying - well, gliding, really - since long before Samuel L. Jackson had had it with them.

True flight, actively wing-powered and sustained for lengthy periods of time, has evolved only four times (in insects, pterosaurs, birds, and bats). In contrast, gliding flight (defined as falling at an angle more shallow than 45° from horizontal) is more energy efficient and has evolved many times, and many birds use both gliding flight and true flight depending on the circumstance. Among the vertebrates are found gliding lemurs, squirrels, fishes, frogs, lizards, ants, squids, and of course snakes. Of all the groups that have evolved gliding, snakes would seem to be the least likely candidates, because of their long, cylindrical body that seems ill-suited for flight. But evolve to glide they have. Many gliding groups live in the rainforests of Asia, especially on the island of Borneo, where the trees are very tall and widely spaced, and southeast Asia is where you will find the five species of gliding snake, genus Chrysopelea.

Chrysopelea paradisi

As with many species native to this region of the world, there are a lot of unknowns about gliding snakes. We don't know very much about how they spend their time in the wild, what they eat, or what eats them. Until recently, relatively few scientific papers had been published on Chrysopelea, including a note on their flight in 1906.¹

Jake Socha, a comparative biomechanics researcher at Virginia Tech, studies the gliding flight of Chrysopelea. For his PhD at the University of Chicago, he characterized their mechanism of takeoff, the postures they adopt while gliding, and contributed substantially to our knowledge of their morphology. Socha and colleagues used multiple synchronized video cameras to film and digitally reconstruct the trajectory, speed, and body posture of gliding Chrysopelea, which they frightened off a three-story scaffolding built with a branch sticking out of the side, to simulate a tree. The videos showed that the snakes could descend at a very shallow angle of 13°, comparable to flying squirrels and other accomplished gliding vertebrates.

Next, Socha and colleagues looked for relationships between measures of the snakes' flight performance, such as glide angle and horizontal speed, and morphological characteristics of the snakes. They found that smaller snakes were better able to glide long distances than larger ones, and that the wave amplitude of the snake's body was a more important predictor of flight behavior than its wave frequency, the latter of which they hypothesize helps maintain stability during flight.

Undulating behavior of gliding Chrysopelea

In order to transform their bodies from fairly non-aerodynamic cylinders into a more aerodynamic wing-like shape that generates lift, Chrysopelea can flatten their body by extending their ribs, an observation first made by Robert Shelford (also the first person to document their gliding behavior, in 1906). The flattening process proceeds from anterior to posterior, does not include the tail, and takes only 100–350 milliseconds to complete. Although the exact mechanism of rib expansion has not been examined, it is presumably similar to that used by cobras to spread their hoods. Because the rib muscles are also involved in breathing, it is likely that Chrysopelea cannot breathe when gliding, which could physiologically limit the duration of their glides.

Figure from a 1906 paper describing the change in shape of the body of Chrysopelea.

Finally, Socha and colleagues have investigated Chrysopelea's take-off behavior in great detail, using the same synchronized camera set-up they used to film the snakes in flight. I won't go into excruciating detail (you can read the whole paper here), but you can get an idea of the movements involved by looking at the beautiful images produced below.

So far, the five species of Chrysopelea are the only known gliding snakes, although anecdotal reports suggest that their close relatives, the Bronzeback Snakes in the genus Dendrelaphis, are also capable of making gliding leaps. Although Chrysopelea have been known since the time of Linneaus (who described only their color, as "green, with a yellow line on both sides"), we are still learning about them today, and will probably never know all there is to know. In addition to having a fascinating natural history, these snakes are also incredibly graceful and beautiful. I think I would like to see one in the wild more than just about any other snake, which is always a bold statement to make. One day... 

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1 The author, Robert Shelford, was brought dead specimens of Chrysopelea in the late 1890s by Dyak villagers in inland Borneo, who told him that they were of a flying species. Skeptical, he obtained some live specimens and tested them by dropping them from heights of 15-20'; "after one or two false starts the snake was felt to glide from the experimenter's hands".

ACKNOWLEDGMENTS

Thanks to photographers Angi Nelson and Jake Socha. If you have more questions about Chrysopelea, check out Jake Socha's Chrysopelea FAQ.

REFERENCES

Shelford R (1906) A note on "flying" snakes. Proceedings of the Zoological Society of London 76:227-230

Socha JJ (2002) Kinematics: Gliding flight in the paradise tree snake. Nature 418:603-604

Socha JJ (2006) Becoming airborne without legs: the kinematics of take-off in a flying snake, Chrysopelea paradisi. Journal of Experimental Biology 209:3358-3369 <link>

Socha JJ (2011) Gliding flight in Chrysopelea: Turning a snake into a wing. Integrative and Comparative Biology 51:969-982 <link>

Socha JJ, LaBarbera M (2005) Effects of size and behavior on aerial performance of two species of flying snakes (Chrysopelea). Journal of Experimental Biology 208:1835-1847 <link>

Socha JJ, O'Dempsey T, LaBarbera M (2005) A 3-D kinematic analysis of gliding in a flying snake, Chrysopelea paradisi. Journal of Experimental Biology 208:1817-1833 <link>

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