Herbivores can cause dioecious plants to partly swap sex

Dioecious plants have male or female flowers depending on the individual, but sex expression is not fixed, according to research by Nora Villamil and colleagues. They have found that sex expression in Mercurialis annua (Euphorbiaceae) can be ‘leaky’ when attacked by herbivores. The findings could help explain shifts in mating systems between dioecy having male and female plants and monoecy, having male or female flowers on the same plant.

Flower evolution can be driven by interaction with pollinators, but Villamil and colleagues point out that herbivory can also affect reproduction. They write: “Herbivores can affect sex allocation patterns either directly via plant size or indirectly via effects on pollinator behaviours. By reducing plant size and resource availability, herbivory in dioecious populations may directly increase mortality of individuals with the more costly sex function, potentially leading to or enhancing sex ratio biases.”

The botanists carried out a couple of experiments on both male and female M. annua plants with different levels of herbivory. They then compared how many male and female flowers the plants produced compared with the undamaged plants to see how leaky the sex expression was.

In both cases, herbivory increased the chances of a plant producing flowers of the opposite sex. This difference had reproductive consequences, with males under high herbivory producing many more seeds. Females under herbivory were more likely to produce male flowers, with the larger females being more likely to have male flowers. Females were more likely to be leaky than males, a finding that Villamil and colleagues find odd.

“While leakiness in sex expression can affect both sexes of dioecious species, generally males are more likely to be leaky than females, a pattern that may reflect incomplete transitions from hermaphroditism to dioecy via gynodioecy, with males retaining a residual female function… Against this background, the greater probability of leakiness in females of M. annua is unusual. Our results confirm greater leakiness in females than in males in M. annua, and they also indicate that under simulated herbivory this pattern of enhanced leakiness is maintained and even accentuated.”

“Our results shed further light on the expression of leakiness in sex expression in M. annua, to our knowledge the only plant to date whose leakiness has been investigated experimentally in quantitative terms, showing that antagonists can affect this reproductive trait.”

READ THE RESEARCH

Nora Villamil, Xinji Li, Emily Seddon, John R Pannell, Simulated herbivory enhances leaky sex expression in the dioecious herb Mercurialis annua, Annals of Botany, Volume 129, Issue 1, 1 January 2022, Pages 79–86, https://doi.org/10.1093/aob/mcab129