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Monday, April 9, 2012

Asymmetrical snakes

Pareas margaritophorus
Animals have a long tradition of being bilaterally symmetrical - that is, of the left side and the right being nearly identical. Sure, there are a few exceptions - the human heart is nearly always farther to the left side, for instance. Snakes and other elongate, limbless animals sometimes stagger their paired organs (gonads, kidneys) so that one is in front of the other, to better fit in their cylindrical bodies. Most snakes have even done away with one of their two lungs. But the basic external body plan, the bones and muscles on the left and the right, are always mirror-images of one another, right?

Enter the pareatid snakes. This is a small group of colubroid snakes that relatively recently gained their family status - prior to 2005 they were, like many snakes, considered a subfamily of the Colubridae. Several phylogenetic analyses have found Pareatids to be only distantly related to other colubroids, having diverged from them at least 40 million years ago.

In any case they are incredibly unique. Distributed in tropical southeastern Asia, west of Wallace's line, they are relatively small terrestrial and arboreal snakes that feed mainly on slugs and snails (gastropods). In this respect, they are convergent with some Neotropical snakes, such as species of Dipsas, Sibon, Sibynomorphus, and Tomodon, as well as the African genus Duberria and the familiar North American snakes Storeria and probably Contia. However, pareatids possess a morphological adaptation to gastropodophagy (specifically, cochleophagy) unrivaled in the snake suborder. You see, most snails' shells coil in a clockwise direction from the center of their shell - that is, to the right. This is referred to as dextral, as opposed to sinistral (to the left or counterclockwise). If that seems weird, consider that about 90% of people also have an asymmetry: they are right-handed. This predominance is even reflected in our language: dextral comes from the Latin word dexterous, meaning manual skill, whereas the evil or unlucky connotation of sinistral is reflected in the word sinister. 

That's one sinister snail

So what does this mean for a snail specialist predator? It means that there is a selective force acting on one side of the snake's feeding apparatus, but not the other. Perhaps it goes without saying, but snakes have no hands, so they feed with their mouths only. Specifically, pareatids use their lower jaws to extract snails' soft bodies from their shells, because they lack the crushing bite force of mammals and other snail predators (but wait for my upcoming article on the snake Fordonia leucobalia).

A group of scientists from Kyoto and Shinshu Universities and the Japan Science and Technology Agency noticed this (one species of Pareas is endemic to the Ryukyu Islands of Japan) and decided to investigate museum specimens of pareatids for evidence of asymmetry in their jaws. So as not to damage the specimens (which are from an area of the world where specimens are hard to come by), they used X-ray photography to count the teeth in each mandible (lower jaw). Here's what they found:

Mandibles (lower jaws) of Pareas iwasakii 
Dorsal view of skull of Pareas iwasakii

These are two X-ray photographs of the skulls of Pareas iwasakii, from two papers published in Biology Letters and Nature Communications. The white bars are 10 mm long, for scale. If you didn't notice, count the teeth on the left and right jaws. That's right - way more on the right mandible. Which way did most of those snail shells coil again? Well, what if those two skulls were just weird?

Data from Pareas iwasakii

Data from 297 specimens

Ok, data from almost 300 snakes, including all 14 then-known species of pareatids (a 15th, Pareas nigriceps, was described in 2009). Now I'm convinced. The asymmetry index they calculated is based on the difference in the number of teeth between the left and right mandibles. If you did this in any other group of animals, you would have found that every individual had an asymmetry index between -1 and 1 - that is, an equal number of teeth in the left and right mandibles (imagine a deviation of ±1 if you had, say, a wisdom tooth erupt on one side but not the other). But pareatids had an average of 17.5 teeth in their left mandible and 25 teeth in their right mandible! The two species with asymmetry indices closer to 0 (Aplopeltura boa and Asthenodipsas malaccanus) are known to be slug or lizard-eating, rather than snail-eating, so you would expect different evolutionary pressures on their tooth number because slugs and lizards don't have to be scraped out of asymmetrical shells (which the snail-eaters can accomplish in as few as 24 seconds per snail!).

Aplopeltura boa

Asthenodipsas malaccanus

The authors weren't satisfied to stop there (scientists rarely are). They also did a manipulative experiment. They found a species of snail that had both dextral (clockwise) and sinistral (counterclockwise) morphs, and conducted feeding trials to see which were easier for the asymmetrical snakes for eat. Because these snakes feed nocturnally, they recorded the feeding trials with an infrared camera. This is also a good idea in behavioral experiments because it prevents the observer from unintentionally influencing the actions of the animals being studied merely by their presence.

Analysis of the tapes showed that dextral snails were easily eaten, whereas the snakes had considerable difficulty striking and holding onto sinistral snails. The snakes did not adjust their behavior when confronted with a sinistral snail, so as a result most of the sinistral snails escaped, whereas most of the dextral snails were successfully eaten. You can watch the video of a snake successfully attacking a dextral snail here, and the one of a snake struggling with and eventually dropping a sinistral snail here.

Stills from the video

Not only does this feeding adaptation benefit the snakes, but it has actually been shown to drive speciation in the snails. Because pareatids are so well-adapted for eating dextral snails, sinistral snails are at a significant survival advantage in regions where pareatids occur. Incompatibility between dextral and sinistral snails during mating has prevented both forms from occurring simultaneously, and the dextral form seems to be predominant. It isn't that there is an advantage to being dextral over sinistral - it's just that they all had to be either one or the other in order to be able to mate compatibly, and dextral is just what they all happened to be. But the same researchers who did the first study, plus some of their colleagues from Japan's Tohoku University in Japan and Taiwan's Taipei Municipal University of Education and National Taiwan University, discovered that right-left reversals in shell chirality were under the control of a single gene, so that changes in the allele of that gene could result in immediate speciation. The reason that speciation is immediate is the reproductive incompatibility, and therefore isolation, between dextral and sinistral snails. As long as there are a few other sinistral snails around to mate with (snails are hermaphrodites, so they aren't picky about things like sex), the new sinistral species can take off, free from predation by slug snakes, who cannot grip them with their dextral-snail-adapted jaws. Of course, it's probably only a matter of time before one or more of the slug snakes evolves a sinistral-adapted jaw, but it isn't as quick as it is for the snail because tooth and jaw development are controlled by more than just a single gene. However, the selection in favor of a sinistral-adapted snake jaw will continue to grow as the frequency of sinistral snail species increases. Already, southeast Asia harbors more sinistral snail biodiversity than any other region (12% as opposed to 5% worldwide), likely in part due to selection against dextral and for sinistral shells from snake predation.

Satsuma is one of the snail genera examined

The red lineages are the sinistral snails, many are sympatric with pareatids 

This hypothetical frequency-dependent reversal of snake jaw asymmetry is intriguingly similar to the situation with Lake Tanganyika cichlid fishes. One species of cichlid, Perissodus microlepis, eats the scales off other fishes. It sneaks up from behind and has an symmetrical mouth that allows it to grab scales from either the left or the right side of the prey fish - right-handed individuals snatched scales from the prey's left side and vice versa. Frequency-dependence of prey alertness causes the predominant form of P. microlepis to oscillate between dextral and sinistral. So when dextral P. microlepis predominate, the prey fishes are especially wary of attacks from the left side, and the few P. microlepis with sinistral mouths have an advantage. Eventually, more P. microlepis survive that are sinistral, prey wariness shifts sides accordingly, and the process reverses. You could imagine this happening with pareatids and snails, albeit much more slowly.

Dextral P. microlepis on top, sinistral P. microlepis on bottom

Interestingly, directional asymmetry of the snail-feeding apparatus has been found in other gastropodovores, such as crabs and other aquatic invertebrates. But, even among other snake species that specialize on snail prey in North America, South America, and Africa, pareatids are the only group of snakes to have evolved asymmetric jaws. Perhaps it has something to do with the ontogeny of their feeding - that is, how what they eat changes from when they're young to when they get old. The authors found no differences in the asymmetry index with body size, so small snakes were as asymmetrical as large ones. You might also have noticed that the X-ray of the skull on the right above was from an unhatched pareatid embryo, indicating that asymmetry is an innate, rather than an acquired, trait. This means that baby pareatids must also eat dextral snails - and in fact this was shown experimentally, by Masaki Hoso, who hatched some eggs of Pareas iwasakii in captivity and fed them baby snails. While he couldn't observe the babies feeding on snails directly (they feed at night, remember?), he found the empty shells they left behind.

Oh, the carnage
So although other snakes feed on snails as adults, they might not do so as juveniles, so selection might not be as strong on their jaw asymmetry. Of course, it could also be that pareatids have been feeding on snails for longer than these other lineages (they probably are the oldest lineage of snail-specialist snakes, although fossils are apparently unknown), or that they are more specialized on snails than the other groups, or that some kind of evolutionary constraint keeps the other snake groups from evolving asymmetry.

I'll leave you with a few photos of the other species of pareatids, which are as graceful and beautiful as they are evolutionarily intriguing.

Asthenodipsas laevis from Malaysia

Aplopeltura boa from Borneo

Pareas formosensis from Taiwan

Pareas carinatus from Laos
For more information about current research on pareatids and their prey, see Dr. Masaki Hoso's webpage.



Götz M, 2002. The feeding behavior of the snail-eating snake Pareas carinatus Wagler 1830 (Squamata: Colubridae). Amphibia-Reptilia 23:487-493.

Hirata T, Ota H, 1993. Predation on snails by the pareatine snake Pareas iwasakii. Japanese Journal of Herpetology 15:90-91.

Hori M, 1993. Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216-219

Hoso M, 2007. Oviposition and hatchling diet of a snail-eating snake Pareas iwasakii (Colubridae: Pareatinae). Current Herpetology 26:41-43.

Hoso, M., T. Asami, and M. Hori. 2007. Right-handed snakes: convergent evolution of asymmetry for functional specialization. Biology Letters 3:169-172. <link>

Hoso M, Hori M, 2006. Identification of molluscan prey from feces of Iwasaki’s slug snake, Pareas iwasakii. Herpetological Review 37:174–176.

Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M, 2010. A speciation gene for left-right reversal in snails results in anti-predator adaptation. Nature Communications 1:133.

Ota H, Lin JT, Hirata T, Chen SL, 1997. Systematic review of colubrid snakes of the genus Pareas in the East Asian Islands. Journal of Herpetology 31:79-87.

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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.

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