Big-headed tiger snakes support long-neglected theory of genetic assimilation

Tiger snakes are a group of extremely venomous serpents found all over the southern half of Australia, and on many of its islands. Some were cut off from the mainland by rising sea levels more than 9,000 years ago, while others were inadvertently introduced by travelling humans and have been around for less than 30 years.

When the snakes first arrive on an island, they find prey that are generally larger than they're used to on the mainland. That puts them under strong evolutionary pressure to have larger heads, in order to swallow larger meals. But by feeding snakes from different populations with prey of varying sizes, Fabien Aubret and Richard Shine have found that the more recent immigrants solve the need for larger heads in a very different way than the long-term residents. 

Young populations do it by being flexible. If growing tiger snakes from newly colonised islands are fed on large prey, their heads rapidly enlarge to cope with the sizeable morsels. This flexibility is an example of "phenotypic plasticity" and it doesn't involve any genetic changes.

But Aubret and Shine found that older populations lack this flexibility - they have larger heads from birth and the size of the prey they eat doesn't affect the way they grow. These adaptations are fixed in their genomes. In the heads of tiger snakes, Aubret and Shine have found evidence for a 67-year-old concept in evolution called "genetic assimilation", which has very rarely been tested and is often neglected.

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Its name might conjure up images of science-fiction and DNA-stealing aliens, but genetic assimilation simply describes a means of adaptation. It was proposed in 1942 by Conrad Waddington, who suggested that species initially cope with fresh environments by being flexible - through plasticity. All species have a certain amount of variation built in to their developmental program, which they can exploit according to the challenges they face. In this case, the tiger snakes can grow larger heads if they encounter bigger meals.

But as populations face constant evolutionary pressures, natural selection eventually favours genes that produce the same results, the ones that plasticity once achieved. This is the crux of Waddington's theory - in time, natural selection eliminates plasticity by fixing genes for the same traits. Such genes as said to be "canalised".

Back in the 1950s, Waddington demonstrated this using fruit flies. He exposed developing flies to ether vapour and found that some developed a second thorax (the middle segment between the head and abdomen). By anyone's standards, that's a radical change, but one that was triggered by an unusual environment. Over time, Waddington selectively bred the double-thorax individuals and exposed each new generation to ether. After 20 rounds of this, he found that some flies developed a second thorax naturally, without being exposed to ether. The double-thorax trait, which was initially induced by the environment, eventually became governed by the fly's own genes.

It was a neat idea, but finding other natural examples has been very tricky. Aubret and Shine thinks that genetic assimilation tends to happen over such short timescales (geologically speaking) that you can only really detect it under unusual circumstances. And the spread of tiger snakes across Australia certainly fits that bill.

Aubret and Shine's experiments show that snakes from newly colonised areas had the greatest degree of plasticity when it comes to head size while those from the longest-colonised islands had the least. These differences become abundantly clear when you compare snakes from three populations.

Tiger snakes have only been on Trefoil Island for 30-40 years and the jaws of their hatchlings are still small. However, they're also plastic - if they eat big meals, they'll grow bigger. On Carnac Island, tiger snakes have been around for 90 years and there, the hatchlings have moderately sized jaws and a relatively high degree of plasticity. On Williams Island, the tiger snakes have been cut off from the mainland for 9,100 years and their jaws are not only large from birth but their growth has very little plasticity. 

The differences between the Trefoil and Carnac serpents are particularly interesting, because they suggest that the process of genetic assimilation can take place over a very short span of time, as others have predicted. It starts manifesting within just a few decades, even in animals like tiger snakes that only breed after their second or third birthday. This rapid pace could explain why it's very difficult to observe this process in the wild.

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Reference: Current Biology 10.1016/j.cub.2009.09.061

Images: Tiger snake by Ian Fieggan

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Probably some of the most dangerous caliper work around, that is measuring tiger snake heads.

The obvious question is what maintains phenotypic plasticity before canalization? Why did the snakes on the mainland not settle into having smaller heads without the plasticity? Maybe the mainland is more variable while island prey are constant in size?

Ditto Lilian Nattel's question.

With the snakes, I could imagine that canalization for larger heads might be selectively advantageous over plasticity. With plasticity, there's probably some danger that the young snake can't grow its head fast enough, so it doesn't get enough food to survive & reproduce. Genetic big-heads presumably avoid that selective pressure.

But how is the double-thorax example explained? If the ether merely causes double-thorax as some weird developmental anomoly, why would double-thorax mutations arise? The only thing I can think of is that the double-thorax phenotype is somehow advantageous in the presence of ether. If so, initial exposure to ether merely selects for the occasional non-genetic developmental anomoly that helps the fly survive the ether. Over time, genetic mutations that cause double-thorax could be selected if they were more advantageous than the developmental anomoly.

Has anyone looked into that?

The only thing I can think of is that the double-thorax phenotype is somehow advantageous in the presence of ether.

Can't imagine how. The question is: is that mutation more common in ether than in the wild?

By David MarjanoviÄ (not verified) on 30 Oct 2009 #permalink

David,

Even if it's more common in ether, it's hard for me to see how that explains the observed canalization. What is the likelihood that ether just happens to promote both double-thorax as a developmental anomoly, AND mutations that cause 'constituitive' double-thorax?

The only way I could see that as a credible possiblity is if the apparent developmental anomoly actually results from mutations in relevant somatic cells during early development.

I guess I could stop being lazy and actually try to look at the research. ;-)

Nah, no somatic mutations involved in the ether thorax thing - you're looking at depressed Hox signals. Provided intraspecific variation in the strength of Hox secretion, breed for a drop and soon enough you don't need the ether because the natural secretion's fallen below the threshold. Bingo bongo.

'Genetic assimilation' seems like the closest thing yet to a real-world example of the Baldwin Effect, where a learned behavior gets fossilized into the genome of a population. Here's hoping that's next!

"All species have a certain amount of variation built in to their developmental program, which they can exploit according to the challenges they face".

I like how that sounds, a lot. I apologize if my scientific literature doesnt fit in here, but we are asked every week to review this website for Genetics class, and sincerely Im in love with this site.

By Steffano Mottl (not verified) on 31 Oct 2009 #permalink

You're asked to review this website for Genetics class? That's AWESOME! Can you tell me more?

Hm... I first read about this study in a book about epigenetics. They didn't mention Wattington's theory at all. It also didn't mention that there was a type of tiger snake that couldn't change its jaw size. It is difficult for me to comprehend the idea of epigenetics because of the many theories that relate to the idea, or sound similar, but are not the same.

If the island snakes were left on the mainland for 30 years do you suppose they'd start to develop plasticity as well? You'd think it would be a two way street. Have they identified differences in genes that are more "plastic" compared to the ones that are canalized? Or is that difference outside the genes... perhaps explained by epigentic processes? Agh, so confused! It's great.

Qetzal: in this case, the selective pressure was not advantage, but an individual by the name of Conrad Waddington, who was artificially selecting the double-thorax flies.

If anyone's ever read the Science of Discworld books, they discuss this concept in their section on folk genetics, and use the example of Thalidomide babies. When two Thalidomide-affected adults have a child, the child has a greater chance of having the same defects as if they had been exposed to Thalidomide. This is not due to a mutation caused by Thalidomide, but to the natural mutations that made these people susceptible to Thalidomide's effects in the first place coupled with the human breeding patterns which lead individuals to seek mates that share their weirdness. These mutations initially needed an environmental stressor like Thalidomide to lower the threshold, but with two parents with such genes (which are quite rare; the rate of birth defects with Thalidomide was actually fairly low, with millions of users producing less than 20000 cases of birth defects worldwide) the threshold is lowered such that natural stressors can do the same job as Thalidomide.

Though, to me, this does look like just a restatement of the good old variation->selection->speciation deal.

So are tiger snakes the result of a dehydrated toad mating with another species - such as a tiger...?!

I agree with the first three posters, regarding questioning what maintains the plasticity in the mainland population once canalization sets in. Also, I'm curious what mechanism(s) triggers activation of plasticity once the young snake is in the new environment with larger prey; and at what age or developmental stage the snake is simply too old to have the plasticity function kick in.

Some Tiger Snakes were inadvertently introduced by travelling humans? How does that happen? Did they sneak a lift in a suitcase or the back of boat, or maybe hide inside someone's clothing... a whole new meaning for the word trouser snake. Those things are big and lethal, I'm surprised anyone took it for a ride without realising. Maybe that's just what they told customs.