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Shape-Shifters

Tiger snakes on Chappell Island

Tiger snakes on Chappell Island have rapidly evolved large heads, enabling them to swallow whole mutton bird chicks. Photo © Ben Twist, used with permission.

By Michael Lee & Kate Sanders

Genetic analyses reveal that Australia’s land and sea snakes have rapidly evolved different body shapes and sizes to suit the local prey available, from fat muttonbird chicks to eels hiding in narrow crevices.

Snakes, being universally long and legless, would seem to have little latitude to vary their body shape. However, this apparent uniformity masks a lot of more subtle variation. Tree-dwelling snakes have thin, threadlike bodies with long tails, while ambush predators typically have thick stubby bodies and relatively short tails. Some of the most remarkable body shapes are found in sea snakes: most have ribbon-shaped bodies and paddle-like tails, and many have comically-tiny heads.

All living sea snakes are highly venomous, being descendants of dangerous front-fanged terrestrial snakes that probably resembled tiger snakes and marsh snakes. Their powerful venom enables them to subdue large and often spiny fish prey, and a large head would be very useful for swallowing such items.

However, many sea snakes instead have an anatomical innovation called “microcephaly”, with such remarkably tiny heads and necks that they look like a photoshop morph or a bizarrely proportioned child’s drawing.

Microcephalous sea snakes use their narrow front ends to probe the small burrows of sand eels, which are inaccessible to their large-headed counterparts. This is clearly a very successful foraging strategy: a comprehensive genetic study of sea snakes has shown that microcephaly has evolved convergently in about ten separate lineages of sea snakes, which is much more frequently than previously suspected.

More remarkably, our most recent DNA study has revealed that microcephaly has not just evolved repeatedly but also extremely rapidly – at least in one Indo-Australian sea snake lineage. We found that the blue-banded sea snake (Hydrophis cyanocinctus), which has a normal-sized head, is genetically almost indistinguishable from the co-occurring black-headed sea snake Hydrophis melanocephalus, which has a tiny head and thin neck.

In fact, a superficial assessment of the genetic data would conclude they are the same species. However, this is most unlikely given the extreme anatomical disparity between these two sea snakes: the microcephalous black-headed sea snake is not only a totally different shape but is also half the size of the blue-banded sea snake.

When we performed additional genetic analyses and examined additional genes we concluded that they are most probably “sibling species”: two populations that have only very recently stopped interbreeding, and are beginning their evolutionary journeys towards separate species.

Given that blue-banded and black-headed sea snakes were a single uniform species (probably large-headed) until very recently, the black-headed sea snake must have evolved its tiny head and neck, and reduced its body size, very rapidly. These changes probably occurred within the last few hundred thousand years (and probably much more recently) – a blink in geological time.

Living sea snakes were not the first group to hit upon this evolutionary strategy. One hundred million years ago, during the height of the dinosaur age, the oceans were also filled with snakes, but these represented an entirely separate marine invasion to living sea snakes. These Cretaceous marine snakes were among the most primitive of snakes, retaining tiny hind legs and primitive skull features lost in all other snakes.

Some of these ancient sea snakes had relatively normal proportions, but others, such as metre-long sea serpents called pachyophiids, had a miniscule head and narrow neck. Although modern sand eels almost certainly had not even evolved when pachyophiids lived, there must have been similar burrowing or crevice-dwelling creatures that they could ferret out. Even the most primitive snakes, it would seem, could readily evolve tiny heads and necks to exploit difficult prey.

The ability to rapidly evolve different head shapes as well as body sizes in response to novel prey is not restricted to marine snakes but appears to be a fairly general capability found across all snakes, including terrestrial forms. Research by Rick Shine (University of Sydney), Scott Keogh (Australian National University), Ben Phillips (James Cook University) and colleagues has documented many intriguing examples from Australian land snakes, which include the deadliest snakes in the world and – coincidentally - the nearest relatives of living sea snakes.

Tiger snakes (Notechis scutatus) marooned on islands by rising sea levels are among the most impressive shape-shifters. On tiny windswept Chappell Island in Bass Strait, adult snakes must swallow whole muttonbird chicks to survive. To tackle such large mouthfuls, these tiger snakes evolved to become bizarre giants: twice the size of typical mainland tiger snakes, and with grossly enlarged heads and jaws.

In contrast, on Roxby Island off South Australia, the only prey are small lizards and the tiger snakes have accordingly become dwarfs – perhaps all the better to follow prey down narrow crevices.

These profound changes have evolved within 10,000 years, after rising sea levels cut off these islands (and their resident snakes) from the mainland. Accordingly, despite their bizarre and varied appearances, all island snakes are genetically almost identical to their mainland relatives.

Intriguingly, island snakes seem to have evolved not just different morphologies but also increased “phenotypic plasticity”: a greater ability to tailor growth to suit the surrounding environment. Baby island tiger snakes fed large prey items grow larger jaws, but this effect is weaker in mainland forms.

The cane toad invasion has precipitated an even more recent evolutionary experiment in snake evolution. Rhinella marinus (formerly Bufo marinus) is highly toxic, and snakes with large heads and/or small body sizes are most at risk of ingesting a lethal dose. Red-bellied blacksnakes (Pseudechis porphyriacus) feed mostly on frogs and toads, and are also highly vulnerable to toad poison. In areas now occupied by cane toads, they have adapted by evolving slightly smaller heads and larger body sizes to reduce the chance of them swallowing a fatal meal.

Cane toads were introduced to northern Queensland in 1935, so these subtle but noticeable changes have evolved within a few decades. In contrast, snakes that are highly resistant to toad venom, such as keelbacks (Tropidonophis mairii), would be under far less selective pressure to reduce their vulnerability to toad poisoning, and accordingly do not show evolutionary changes in head or body size.

The ability of snake populations to rapidly change head and body shape to exploit new and challenging prey is likely to facilitate speciation: the fission of a single homogenous species into two separate, non-interbreeding species. For instance, sea snake populations evolving microcephaly to probe eel burrows will have much smaller heads, as well as smaller overall body sizes and different foraging habits, to their large-headed ancestral populations.

A tendency to mate with individuals of similar shape and size – termed “assortative mating” – could initiate the development of reproductive isolation. Such mate preferences might not even be required: large-headed and small-headed morphs often have different foraging strategies and grounds, and thus probably encounter potential mates of the same “type” more frequently than individuals with divergent shapes and habitat preferences.

Our genetic work indeed suggests that changes in head and body sizes are linked to speciation. Further field and captive studies are planned to explore the behavioural and ecological factors that potentially promote reproductive isolation in these species.

Snakes are the most rapidly speciating reptiles, with more than 3500 described species. Colubroid snakes, which include all the snakes mentioned here, are the most rapidly speciating snakes, and sea snakes are the most rapidly diversifying colubroids: truly the fastest of the fast. The ability to quickly evolve new head and body shapes to exploit novel prey has likely been a key ingredient of their evolutionary success, with Australian snakes providing some of the most “striking” examples.

Michael Lee is a senior research scientist at the South Australian Museum and University of Adelaide. Kate Sanders is an ARC postdoctoral research fellow at the University of Adelaide.