Life history tradeoffs form the foundation for understanding trait evolution, constraints, and how organisms interact with their abiotic and biotic environment. For plants, tradeoffs have played a central role in understanding the diverse strategies employed for defense against insect herbivores. Classic plant defense theory posits that resource availability imposes growth-defense tradeoffs among species. Species adapted to low-resource environments grow slowly but are highly defended, whereas species adapted to high-resource environments grow fast but have lower levels of defense. These same trade-offs are predicted to occur within species and affect optimal physiological strategies. Yet, among populations, there can be substantial variation in plant defense, and growth and defense do not appear to be negatively correlated. Recent work suggests that growth and defense are often positively correlated across populations, in opposition to existing theory (Hahn & Maron 2016 TREE). Understanding of what drives the substantial population-level variation in plant defense remains poor. This represents an important knowledge gap and impedes developing a more synthetic framework for understanding the evolution of plant defense.
In collaboration with John Maron (U Montana) and Anurag Agrawal (Cornell), we tested the above framework using the perennial native forb showy milkweed (Asclepias speciosa), a species that inhabits a strong climate gradient from Washington to Minnesota. In natural populations, abundance and damage by a specialist cerambycid beetle (Tetraopes femoratus) increased towards warmer sites with longer growing seasons. Growth and defense traits showed strong positive relationships with climate and were positively correlated. In a common garden, correlations between traits and climatic conditions at the site where the populations originated were only recapitulated for defense traits (i.e., latex and toxic cardenolides), suggesting defensive traits are genetically differentiated among populations. Correlations between growth and defense traits were also weaker and more negative in the common garden compared to the natural populations. Taken together, these data suggest that a strong climate gradient and co-varying herbivore pressure likely shape the positive correlations among traits, with climatically favorable sites likely facilitating the evolution of greater defense at minimal costs to growth (Hahn et al. 2019 Am Nat). This study provides an alternative lens through which to view costs and benefits of defenses, because the positive correlations between growth and defense demonstrated here is the opposite of the growth-defense tradeoff that underpins much inter- and intraspecific plant defense theory.
A newly funded NSF project (DEB-1901552) in collaboration with John Maron (U Montana) will test the generality of how the abiotic environment mediates plant growth, defense, and insect herbivore pressure among populations of co-occurring grassland plant species. We hypothesize that, in opposition to current theory, the resource environment along with associated changes in herbivore pressure results in the evolution of positive growth-defense correlations among populations. Testing this hypothesis will involve reciprocally transplanting individuals of six co-occurring focal species from replicated populations that occur within high- and low-resource regions into common gardens within each region. Growth and defense traits (i.e., evaluated via chemical analysis and insect performance assays) will be measured in common gardens to determine the extent to which growth and defense correlations are positive, and whether traits are genetically differentiated among populations or driven by plastic responses to environmental conditions. Surveys of insect abundance, damage, and fitness-effects on plants will also be conducted at the field sites. Ultimately, this multispecies approach will help to generalize understanding of the factors driving intraspecific growth-defense correlations; patterns that clearly differ from current predictions in plant defense theory.