At the Edge of Invasion, Possible New Rules for Evolution

Just as Galapagos finches are icons of evolution by natural selection, Australia’s cane toads may someday be icons of “spatial sorting” — a dynamic that seems to exist at the edges of invasion, altering the standard rules of evolution. Cane toads have evolved in odd ways Down Under. Adaptations that drove their dramatic spread made […]

Just as Galapagos finches are icons of evolution by natural selection, Australia's cane toads may someday be icons of "spatial sorting" -- a dynamic that seems to exist at the edges of invasion, altering the standard rules of evolution.

Cane toads have evolved in odd ways Down Under. Adaptations that drove their dramatic spread made individual toads less reproductively fit. Evolution through natural selection of hereditary mutations still exists, but no longer appears driven by reproductive imperatives alone. It's also shaped by speed.

"The possibility that some traits have evolved by 'mating betwixt the quickest' rather than 'survival of the fittest' warrants further attention," wrote biologists led by the University of Sydney's Richard Shine in the March 21 Proceedings of the National Academy of Sciences.

Introduced to northeast Australia 75 years ago in an ill-advised attempt at beetle control, cane toads spread like fire, their range expanding at rates that grew daily. As they first arrived at his study area, Shine noticed something strange: As expected, the toads displayed myriad adaptations -- longer legs, greater endurance, a tendency to move faster and farther and straighter -- that affected their ability to disperse, but dispersal's benefits were unclear.

>It seemed hard to reconcile with the idea of natural selection enhancing individual fitness. We started thinking about what could have caused them to become such driven little robotic dispersal machines.

The fastest-spreading cane toads also had the highest mortality rates. Longer, stronger toad legs led to spinal injuries. "Most obviously, why did the toads just sprint through our magnificent, food-rich flood plain in a frenetic rush to keep on going?" said Shine. After all, if the toads' evolution is driven solely by a drive to reproduce, they would have stopped to enjoy the spoils of invasion.

"Much of what they did seemed hard to reconcile with the idea of natural selection enhancing individual fitness," said Shine. "We started thinking about what other kinds of processes could have caused them to become such driven little robotic dispersal machines."

In the new study, Shine describes those processes, which fall under the rubric of "spatial sorting" and are most easily understood by analogy: Imagine a race between rowboats crewed by randomly distributed oarsmen. If the race is stopped intermittently, and oarsmen randomly redistributed between boats nearest each other, boats in the lead will accumulate ever-higher proportions of skilled rowers.

Those are the dynamics of spatial sorting. Boats are organisms, rowers are genes and the crew swap is reproduction. Each newly-crewed boat is offspring. Generation by generation, organisms in the lead get faster and faster. Classical natural selection still operates -- if a mutation causes an organism's offspring to go sterile, the lineage soon ends -- but it's no longer the only driver of evolution.

Now space matters, too. Physical proximity produced by dispersal continue to shape that dispersal. Whatever drives creatures to spread farther and faster clusters at the front. If an adaptation improves dispersal but hurts survival, it matters less than usual, because the pool of potential mates is determined by their ability to cover ground.

A key challenge in studying spatial sorting is disentangling the effects of natural selection and spatial sorting. In many cases, better dispersal is a good, old-fashioned adaptation: It might help organisms find new sources of food, or relieve overcrowding.

Such disentanglement is presently hard to do, wrote Shine. Cane toads are the best-studied candidate for spatial sorting, though gaps in data still exist.

But spatial sorting might help explain instances of a phenomenon called preadaptation, in which complex traits emerge through the combination of many smaller adaptations, each of which provides no survival advantages. It would seem unlikely for them to persist long enough to collect in one place -- unless, that is, survival advantages are no longer so important. And in a world full of biological invasions, anything that helps explain their dynamics deserves further study.

"Spatial sorting may prove to be classical natural selection's shy younger sibling, not as important as Darwinian processes but nonetheless capable of shaping biological diversity by a process so-far largely neglected," wrote Shine's team.

Image: Cane toad (Sam Fraser-Smith/Flickr)

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Citation: "An evolutionary process that assembles phenotypes through space rather than through time." By Richard Shine, Gregory P. Brown, and Benjamin L. Phillips. Proceedings of the National Academy of Sciences, March 21, 2011.