Bufotoxin Tolerance in Keelback Snakes: recent adaptation to a new threat, or preadaptation from an ancient foe?

by Allie Wilkinson on November 30, 2010

The spread and current range of the cane toad in Australia.

The cane toad (Bufo marinus) was introduced to Australia in what was another failed attempt at biological control.  The Bureau of Sugar Experiment Stations brought over the first cane toads from Hawaii in June of 1935 in an effort to control the cane beetle, which was destroying the sugar cane crops of northern Queensland.  About  100 cane toads were released in August of that year in northern Queensland, but the little buggers multiplied like crazy and today they number over 200 million and have spread as far as New South Wales and the Northern Territory.  One reason they have been able to multiply so successfully is that they are highly toxic, and are toxic at all life stages.  As a result, cane toads have few predators in Australia. Their rapidly spreading invasion has done serious ecological damage — a preliminary risk assessment of cane toads in Kakadu National Park stated that the predation of the cane toad by native wildlife is the greatest risk to biodiversity.

Notice I said few predators.  Although many snakes in Australia are unable to survive the cane toad’s toxins, one native species- the keelback snake (Tropidonophis mairii), is relatively resistant to the deadly toad toxins and remains common in toad-infested areas.  The toad’s toxins have minimal effects on the keelback snake, but the snake still prefers eating native frogs to the invasive cane toad.  Is the keelback’s ability to coexist with toads a result of its ancestral Asian origins, or the result of rapid evolution since the toads’ arrival– and is it’s preference for frogs vs toads an innate or learned behavior?  That’s what a few Australian scientists were hoping to find out.

Image from jcu.edu.au

In order to assess whether or not the keelback’s feeding preference was innate, the scientists looked at two populations of snakes– one in Townsville, where keelbacks and cane toads have lived together for over 60 years, and the other in Darwin, where the snakes and toads have lived together less than four years.  In one experiment, naive snakes were offered a choice of frog or toad for dinner, and the results were recorded.  In the second feeding behavior experiment, the snakes that co-habitated with toads for a long time were tested as to whether or not feeding behavior was learned by being split into two groups- toad-naive and toad-experienced.  The snakes were fed four meals of experimental treatments, followed by a fifth meal to see how prior exposure to toads influenced the snake’s feeding response.  The toad-naive snakes were offered native frogs for their first four meals, and the toad-experienced snakes were offered frogs and cane toads in an alternating sequence.  For the fifth meal, all of the snakes were offered a cane toad.  The final experiment tested toad-naive and toad-experienced snakes for the physiological tolerance to toad toxins by giving the snakes a dose of toad toxin and seeing how it affected the snakes’ performance as they small around a small pool.

The researchers found that being toad-experienced did not affect the keelback’s tolerance to toxins and that prior experience with toads did not significantly affect the tendency of a young keelback snake to consume a toad, showing that  learning plays little or no role in the keelback’s aversion to toads.  The answer as to why keelback snakes are better able to deal with cane toads than the counterparts lies in the species’ biogeographic origin.  In Asia, keelbacks would have encountered Asian toads, something that Australian snakes would not have experienced, since Australia has no native toads.  These previous encounters between snakes and toads during the Pleistoscene and Miocene would have allowed the keelback to evolve their physiological tolerance to toad toxin, which enabled the current-day keelbacks to be better suited to tolerate the toxins of American toads, since the toxins are similar to those of Asian toads.  The snakes’ aversion to cane toads as prey, and their physiological tolerance to the cane toad’s toxins are pre-existing adaptations from the keelback’s ancestral Asian origins, rather than the result of the rapid evolution of adaptations since the toad’s arrival to Australia.

ResearchBlogging.orgLlewelyn, J., Phillips, B., Brown, G., Schwarzkopf, L., Alford, R., & Shine, R. (2010). Adaptation or preadaptation: why are keelback snakes (Tropidonophis mairii) less vulnerable to invasive cane toads (Bufo marinus) than are other Australian snakes? Evolutionary Ecology DOI: 10.1007/s10682-010-9369-2

This post is a submission in a contest held by NESCent, in which two winners will receive a travel stipend to attend ScienceOnline2011.

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