Can plants escape from an arms race?

How do you fight off attackers if you’re a plant? One way is to build a thicker armour. That triggers the attacker to evolve better methods of penetrating your skin, and you can’t sensibly do that with fresh young material. Maybe you could develop toxins to ward of herbivores, but then herbivores would develop tolerance. So you’d need more difficult toxins, which increases the selection in attackers for guts that can disarm the poisons. You have a plant investing more time and energy in synthesising hard to fight chemicals, and herbivores developing more specialised digestive systems to disarm those defences. Where does it end?

The dogbane family (Apocynaceae), produces a few poisons, including pyrrolizidine alkaloids (PAs). They’re not simple chemicals to make, and they can be dangerous, even to humans. For us, PAs can lead to liver cancer over the years, so imagine what it could do to a tiny caterpillar living on just one plant. Yet, it turns out that some caterpillars can tolerate this plant with no problems. Specialisation has given them the ability to survive the toxin. Worse still, the Danainae, milkweed and clearwing butterflies, actually seek out this plant.

For these butterflies, the arms race has led to them learning to use the toxins for their own benefit. Loading up on PAs makes them poisonous to predators, so not only are the plants failing to fight the caterpillars, they’re actually helping defend their attackers. Some butterflies even use PAs in courtship, to attract females and create more caterpillars. The result is that some plants are spending a huge amount of effort to make their lives worse. That doesn’t seem like a good idea.

Tatyana Livshultz and colleagues have been investigating this problem. They have looked to see if what happens is that plants have a selective pressure to de-escalate their defences and lose the ability to create these compounds.

What they looked for was evidence of an enzyme, homospermidine synthase (HSS), used for creating PAs. What they found were hss orthologues, DNA sequences evolved from a common ancestor, in various Apocynaceae species. Not all of these species could create PAs. Examination of the Apocynaceae shows it only evolved once. That means looking back to see what the latest possible common ancestor was, gives a minimum age for the gene.

While they found only evidence of one origin for hss, Livshultz and colleagues have found evidence that descendants have independently lost PAs multiple times. These events are consistent with the de-escalation hypothesis.

One of the problems with de-escalation is that the reason a plant developed PA synthesis is likely to be around still. Losing PAs doesn’t just reduce attraction to Danainae butterflies, it also removes a deterrent to generalist herbivores. Livshultz and colleagues have a section of their paper asking why so many of the plants they studied had cardenolides and not PAs. It would be interesting to have a close study of the ecosystems where Apocynaceae have lost their PAs, and see if this is due to synthesis and caterpillar infestation being a bigger combined cost to the plant than less effective defences with a wider range of herbivores.

More and bigger weapons might seem like an obvious choice for defence. However, the Apocynaceae seem to be capable of adapting to changing situations and taking the most effective approach to reducing harm, rather than simply amplifying current tactics and hoping the next time will be different.