Plants evolve away from obsolete defences when attacked by immune herbivores

A new study shows that plants can evolve out of their obsolete defence mechanisms when facing an immune enemy, an illustration of the “defence de-escalation” evolution theory.

Do you know what caused soldiers to stop wearing chainmail and steel plate armour?

Armies evolved away from heavy metallic armour because it ceased to be effective against modern weapons, and there was no longer any point in spending resources on it. “Adapt or die,” as the saying goes.

Now, new research from the Academy of Natural Sciences of Drexel University shows that plants also adapt away from obsolete defences.

The study, published in New Phytologist and led by Tatyana Livshultz, PhD, assistant curator of Botany at the Academy and an assistant professor in the College of Arts and Sciences, found genetic evidence that multiple lineages of plants, whose ancestors produced a chemical that may deter herbivores, evolved to stop producing it, potentially as a response to a prime foe’s immunity.

Image: Asclepias syriaca, commonly called common milkweed, butterfly flower, silkweed, silky swallow-wort, and Virginia silkweed. It is in the genus Asclepias, the milkweeds. Source: Wikipedia.
Asclepias syriaca, commonly called common milkweed, butterfly flower, silkweed, silky swallow-wort, and Virginia silkweed. It is in the genus Asclepias, the milkweeds. Source: Wikipedia.

Livshultz and her team traced the evolution of a gene that is involved in the production of a particular class of chemicals. Pyrrolizidine alkaloids, found in the Apocynaceae, a flowering plant family commonly known as the dogbanes and milkweeds, are highly toxic to humans and other mammals. By tracing the gene back, they were able to find out when production of the chemicals first evolved, and how many times it was discontinued.

After identifying a single origin of the gene (and, by inference, the chemicals) in the most recent common ancestor of more than 75 percent of current Apocynaceae species, the researchers found evidence that the gene became nonfunctional (and the chemicals ‘lost’ to evolution) at least four different times among that plant’s descendants.

Looking for a correlation between the gene’s distribution in the plants and interactions with animals unfazed by the defence alkaloids, Livshultz and her team found a significant connection with Danainae (milkweed and clearwing) butterflies.

Almost every species of Apocynaceae eaten by larvae of Danainae is descended from that alkaloid-producing ancestor. Knowing that most species of this lineage of butterflies actually seek out pyrrolizidine alkaloids, it appears that some species in this branch of Apocynaceae may have stopped producing the alkaloids because they were actually attracting milkweed butterflies, not repelling them.

“Pyrrolizidine alkaloids are likely an ineffective defence against Danainae. Furthermore, they are actually beneficial to them since they take in these chemicals for their own defence against their predators,” Livshultz explained.

These findings support the ‘defence de-escalation’ hypothesis: organisms will evolve to stop using precious resources on defence mechanisms if they’re not working anymore.

One benefit of defence de-escalation is potentially diverting resources to defences that do work.

“Apocynaceae species of this lineage produce a number of different classes of defensive chemicals, including cardenolides and other types of alkaloids,” Livshultz explained. “It has been shown that cardenolides are at least partially effective defences against adapted herbivores such as the monarch butterfly.”

Image: An Idea leuconoe, the paper kite butterfly, on the Parsonia alboflavescans. In the inset is the butterfly's larva on the same kind of plant.
An Idea leuconoe, the paper kite butterfly, on Parsonia alboflavescans. In the inset is the butterfly’s larva on the same kind of plant. Source: Livshultz et al.

Why do any Apocynaceae species still produce pyrrolizidine alkaloids? “Perhaps because they suffer more from other insects that are deterred by these chemicals,” Livshultz offered.

Livshultz and her colleagues will further test the hypothesis by reconstructing a very detailed history of the pattern of retention and loss of pyrrolizidine alkaloids in this lineage and ask if exploitation by Danainae is a good predictor of loss.

A better understanding of the dynamics of defence de-escalation is important to understanding co-evolution, the theory that associated species driving each other’s adaptations.

“Co-evolution explains how interactions between species can drive the origin of novelty and diversity,” Livshultz said.

Implications from these theories extend beyond plants to humans.

“Understanding the evolution of plant defences is of practical importance to people, whether we focus on agriculture — herbivorous insects can cause 15 percent reductions in crop yields; medicine — plant secondary metabolites (pyrrolizidine alkaloids are one variety) are an important source of medicinal compounds; or environmental protection — such as developing control strategies for invasive plants,” Livshultz said.

This is an edited version of an original press release by Frank Otto, Drexel University.

Thumbnail: flickr/wplynn, CC BY-ND 2.0

Read the paper: Livshultz, T., Kaltenegger, E., Straub, S. C. K., Weitemier, K., Hirsch, E., Koval, K., Mema, L. and Liston, A. (2018) Evolution of pyrrolizidine alkaloid biosynthesis in Apocynaceae: revisiting the defence de-escalation hypothesisNew Phytologist. doi: 10.1111/nph.15061