Ontogenetic trajectories of direct and indirect defenses of myrmecophytic plants colonized either by mutualistic or opportunistic ant species.

Myrmecophytic plants are expected to produce greater direct defenses when young and switch towards indirect defenses once they reach the size and vigor to produce enough rewards for their ant mutualists. The presence of opportunistic ant species, however, is likely to promote the variation in these ontogenetic trajectories. When plants do not obtain benefits from ants, they cannot rely on this indirect defense. Hence, the expression of direct defenses is expected to remain constant or even increase during the development of plants colonized by opportunistic ants, whereas a reduction in resource allocation to indirect defenses should be observed. To assess if myrmecophytic plants adjust their ontogenetic trajectories in defense as a function of the colonizing ant species, we estimated direct and indirect defenses at four ontogenetic stages of the myrmecophytic plant Vachellia hindsii colonized by either mutualistic or opportunistic ant partners. We report that cyanogenic potential decreased while leaf thickness and the production of sugar in extrafloral nectaries increased along plant development. The magnitude of these ontogenetic changes, however, varied as a function of the identity of the colonizing ants. As expected, when colonized by opportunistic ants, plants produced more direct defenses and reduced the production of rewards. We suggest that facultative changes in the expression of ontogenetic trajectories in direct and indirect defenses could be a mechanism to reduce the fitness costs associated with opportunistic interactions.

Risk of herbivore attack and heritability of ontogenetic trajectories in plant defense.

Ontogeny has been identified as a main source of variation in the expression of plant phenotypes. However, there is limited information on the mechanisms behind the evolution of ontogenetic trajectories in plant defense. We explored if risk of attack, herbivore damage, heritability, and phenotypic plasticity can promote or constrain the evolutionary potential of ontogenetic trajectories in three defensive traits. We exposed 20 genotypes of Turnera velutina to contrasting environments (shadehouse and field plots), and measured the cyanogenic potential, trichome density, and sugar content in extrafloral nectar in seedlings, juveniles and reproductive plants. We also assessed risk of attack through oviposition preferences, and quantified herbivore damage in the field. We estimated genetic variance, broad sense heritability, and evolvability of the defensive traits at each ontogenetic stage, and of the ontogenetic trajectories themselves. For plants growing in the shadehouse, we found genetic variation and broad sense heritability for cyanogenic potential in seedlings, and for trichome density at all ontogenetic stages. Genetic variation and heritability of ontogenetic trajectories was detected for trichome density only. These genetic pre-requisites for evolution, however, were not detected in the field, suggesting that environmental variation and phenotypic plastic responses mask any heritable variation. Finally, ontogenetic trajectories were found to be plastic, differing between shadehouse and field conditions for the same genetic families. Overall, we provide support for the idea that changes in herbivore pressure can be a mechanism behind the evolution of ontogenetic trajectories. This evolutionary potential, however, can be constrained by phenotypic plasticity expressed in heterogeneous environments.

Plant defence as a complex and changing phenotype throughout ontogeny.

BACKGROUND AND AIMS: Ontogenetic changes in anti-herbivore defences are common and result from variation in resource availability and herbivore damage throughout plant development. However, little is known about the simultaneous changes of multiple defences across the entire development of plants, and how such changes affect plant damage in the field. The aim of this study was to assess if changes in the major types of plant resistance and tolerance can explain natural herbivore damage throughout plant ontogeny. METHODS: An assessment was made of how six defensive traits, including physical, chemical and biotic resistance, simultaneously change across the major transitions of plant development, from seedlings to reproductive stages of Turnera velutina growing in the greenhouse. In addition, an experiment was performed to assess how plant tolerance to artificial damage to leaves changed throughout ontogeny. Finally, leaf damage by herbivores was evaluated in a natural population. KEY RESULTS: The observed ontogenetic trajectories of all defences were significantly different, sometimes showing opposite directions of change. Whereas trichome density, leaf toughness, extrafloral nectary abundance and nectar production increased, hydrogen cyanide and compensatory responses decreased throughout plant development, from seedlings to reproductive plants. Only water content was higher at the intermediate juvenile ontogenetic stages. Surveys in a natural population over 3 years showed that herbivores consumed more tissue from juvenile plants than from younger seedlings or older reproductive plants. This is consistent with the fact that juvenile plants were the least defended stage. CONCLUSIONS: The results suggest that defensive trajectories are a mixed result of predictions by the Optimal Defence Theory and the Growth-Differentiation Balance Hypothesis. The study emphasizes the importance of incorporating multiple defences and plant ontogeny into further studies for a more comprehensive understanding of plant defence evolution.