Simulated herbivory enhances leaky sex expression in the dioecious herbMercurialis annua

Abstract

Background and Aims Plant reproductive traits are widely understood to be responsive to the selective pressures exerted by pollinators, but there is also increasing evidence for an important role of antagonists such as herbivores in shaping these traits. Many dioecious species show leaky sex expression, with males and females occasionally producing flowers of the opposite sex. Here, we asked to what extent leakiness in sex expression in M. annua might also be plastically responsive to simulated herbivory. This is important because enhanced leakiness in dioecious populations could lead to a shift in both the mating system and in the conditions for transitions between combined and separate sexes. Methods We examined the effect of simulated herbivory on the sexual expression of males and females of Mercurialis annua (Euphorbiaceae) in two experiments in which different levels of simulated herbivory led to enhanced leakiness in both sexes. Key Results We showed that leaky sex expression in both males and females of the wind-pollinated dioecious herb Mercurialis annua is enhanced in response to simulated herbivory, increasing the probability and the degree of leakiness in both sexes. We also found that leakiness was greater in larger females but not in larger males. Conclusions We discuss hypotheses for a possible functional link between herbivory and leaky sex expression, and consider what simulated herbivory-induced leakiness might imply for the evolutionary ecology of plant reproductive systems, especially the breakdown of dioecy and the evolution of hermaphroditism.

Disentangling the effects of jasmonate and tissue loss on the sex allocation of an annual plant

“…We do not know whether the reaction norm of male-flower production by females in the ancestral dioecious populations is adaptive, but it might be so (Villamil et al, 2021). However, we can safely say that the change in reaction norm that we have observed cannot be adaptive, for two reasons.…”

“…Because the genotypes used in our experiment are females that are now expressing a greatly enhanced leaky male-flower production that has evolved in the absence of herbivory, we had no a priori expectation for how they should respond to simulated herbivory. However, previous work on dioecious M. annua has shown that simulated herbivory enhances leaky sex expression in both males and females (Villamil et al, 2021), for reasons that may or may not be adaptive. We might thus have expected this tendency for greater leakiness under herbivory to have been retained or even enhanced in the genotypes we used in our experiment.…”

“…Our experiment revealed that tissue loss due to chronic simulated herbivory in M. annua caused females with enhanced leaky sex expression in response to recent selection to shift their sex allocation away from male flower production. This response was thus opposed to that of their less leaky recent ancestors, for which tissue damage increased male 10.3389/fpls.2022.812558 flower production (Villamil et al, 2021). In other words, the very direction of the reaction norm of male flower production by females in response to tissue damage in natural populations of dioecious M. annua has been altered by strong selection on male flower production.…”

“…Pollinator-related selection is thought to be a major agent shaping both fixed and plastic aspects of plant sexual systems, but the influence of antagonists has probably been underestimated (Strauss et al, 1996;Carr and Eubanks, 2014;Johnson et al, 2015;Lucas-Barbosa, 2016;Santangelo et al, 2019). Herbivory, for instance, can affect floral display (Strauss et al, 1996;Santangelo et al, 2019), coloration (Strauss et al, 2004;Vaidya et al, 2018), floral scent Ramos and Schiestl, 2019), sex ratios (Hendrix and Trapp, 1981;Krupnick and Weis, 1998;Krupnick et al, 2000;Thomson et al, 2004) and plant sexual expression (Villamil et al, 2021). Moreover, selection on plant mating systems (e.g., through expression of selfcompatibility/self-incompatibility) can influence the evolution of anti-herbivore defenses (Núnez-Farfán et al, 1996;Núñez-Farfán et al, 2007;Campbell and Kessler, 2013).…”