Quoll vs. toad: a toxic brew

A native of Central and South America, the cane toad, Rhinella marina, was introduced to Australia in 1935 with great fanfare. The plan was for the voracious cane toad to eat all of the grey-backed cane beetles that were plaguing sugar cane plantations in northern Australia (a similar introduction had been successful in Puerto Rico).  But the plan failed, in part because there was no cover from predators, so the toads were not enthusiastic about hanging out in sugar cane plantations, and in part because adult beetles live primarily near the tops of sugar cane, and cane toads are poor climbers.

UniToad_BenPhillips

A cane toad. Credit: Ben Philips

So now, northern Australia has a cane toad plague, which is wreaking havoc on ecosystems, and threatening many native species, including the northern quoll, Dasyurus hallucatus. These omnivorous marsupials eat fruit, invertebrates and small vertebrates.  Unfortunately, their long list of food items includes cane toads, which are highly toxic to most consumers, having poison glands that contain bufotoxin, a composite of several very nasty chemicals.  If a northern quoll eats a cane toad, it’s bye bye quoll.

Male captive born northern quoll_EllaKelly

A northern quoll. Credit: Ella Kelly.

Unfortunately most quolls have not gotten the message; huge numbers are dying, and populations are going extinct.  As toads continue their invasion from north to south, more quoll populations, particularly those in northwestern Australia, will be at risk.

KellyFig1

Map of Australia showing past (light shading) and recent (dark shading) northern quoll distribution, and present (solid line) and future (dashed line) cane toad distribution.

Some quolls show “toad-smart” behavior and don’t eat toads. Ella Kelly and Ben Phillips are trying to understand how this happens. This is particularly important because a few quoll populations have managed to survive the cane toad plague by virtue of being toad-smart (though 95% of quoll populations have gone extinct in the wake of the cane toad wave). The researchers reason that if there is a genetic basis to toad-smart behavior, it might be possible to introduce toad-smart individuals into populations that have not yet been overrun by cane toads.  These individuals with toad-smart genes would breed and spread their genes through their adopted population.  This strategy of targeted gene flow would give the recipient population the genetic variation needed, so that some individuals (those with toad-smart genes) would be more likely to survive the cane toad invasion.  Over time toad-smart behavior would spread throughout the population via natural selection.

Targeted gene flow requires the trait to be influenced by genes.  To test for a genetic basis to the toad-smart trait, Kelly and Phillips designed a common-garden experiment, capturing some quolls that had survived the cane toad invasion (toad-exposed), and others from regions that had not yet been exposed (toad-naïve).  At Territory Wildlife Park, Northern Territory, Australia, the researchers bred these quolls to create three lines of offspring: Toad-exposed x toad-exposed, toad-exposed x toad-naïve (hybrids), and toad-naïve x toad-naïve.  They raised these three lines under identical conditions at the park. Kelly and Phillips then asked, are there behavioral differences in how these three lines respond to cane toads?

Kellycagedquoll

Northern quoll captured in Northern Territory, Australia. Credit: Ella Kelly.

The researchers set up two experiments.  First they asked, which would a quoll (that had never before experienced a cane toad) prefer to investigate if given the choice: a dead cane toad or a dead mouse? It turned out that the quoll offspring with two toad-exposed parents were somewhat more interested in mice than in cane toads.  The same was true for the hybrids.  However, the toads with two toad-naïve parents showed little preference.

Second, and more important, the researchers gave quolls from the three lines the opportunity to eat a toad leg (which does not have enough poison to harm the quoll). The results of this experiment were striking; offspring of toad-naïve parents were twice as likely to eat the toad leg than were offspring of toad-exposed parents, or hybrids with one parent of each type.

KellyFig4

Proportion of toad-naive (both parents toad-naive), hybrid and toad-exposed (both parents toad-exposed) quoll offspring that ate a cane toad leg. Error bar = +/- 1 SE.

Kelly and Phillips conclude that toad-smart behavior is a genetically-based trait that has been under strong natural selection in populations of quolls that survived the cane toad invasion.  Hybrid offspring behave similarly to the offspring of two toad-exposed parents, suggesting that toad-smart behavior has a dominance inheritance pattern. The researchers propose using targeted gene flow, in this case introducing toad-adapted individuals into populations prior to the arrival of cane toads. Recently, Kelly and Phillips released 54 offspring with toad-smart genetic backgrounds onto Indian Island, which is about 40 km from Darwin.  The island has a large cane toad population, so the researchers will follow the introduced quoll population to see whether it is genetically equipped to survive in the presence of the cane toad scourge.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kelly, E. and Phillips, B. L. (2019), Targeted gene flow and rapid adaptation in an endangered marsupial. Conservation Biology, 33: 112-121. doi:10.1111/cobi.13149. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

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