Chemical defense over decadal scales: Ontogenetic allocation trajectories and consequences for fitness in a foundation tree species

Abstract

Expression of herbivore defense traits can change dramatically during the course of plant development. Little is known, however, about the degree of genetic or sexual variation in these ontogenetic defense trajectories or whether the trajectories themselves are adaptive, especially in long‐lived species. We used a 13‐year dataset of chemical defense traits, growth and survivorship from a common garden of trembling aspen (Populus tremuloides) genotypes to document long‐term defense trajectories and their relationship to tree fitness during juvenile and early mature stages. Overall, concentrations of the two principal classes of aspen defense compounds (salicinoid phenolic glycosides [SPGs] and condensed tannins [CTs]) decreased to differing degrees in foliage of juvenile trees and then remained relatively constant in maturity. Initial values, juvenile rates of change and average mature values all exhibited significant genetic variation for both SPGs and CTs. Relationships between defense trajectory parameters and metrics of tree fitness (growth and survivorship) depended on compound type and tree sex. Females with higher‐allocation SPG trajectories (high initial juvenile concentrations, slow juvenile declines, high mature concentrations) grew more slowly relative to females with lower‐allocation trajectories. In males, higher‐allocation SPG trajectories had a lesser effect on growth but were associated with reduced mortality. Juvenile CT trajectories were not correlated with tree fitness, but average CT concentration in maturity was positively related to growth in females. These results suggest that ontogenetic defense trajectories are adaptive and subject to natural selection. Genotypic variation and ontogeny shape tree defensive chemistry, both independently and interactively. These patterns of defense expression have the potential to structure trophic interactions and the genetic composition of forests in both space and time. A free Plain Language Summary can be found within the Supporting Information of this article.

Ontogenetic changes in the targets of natural selection in three plant defenses

“…Similarly, changes in the direction and strength of natural selection have been reported for the reef fish Pomacentrus amboinensis , with shifts from favoring small sizes early in their ontogeny to prevent starving, to faster growth in older individuals to reduce predation risk (Gagliano et al , ). In the case of plants, despite the accumulated evidence of changes in plant defensive traits (Senner et al , ) during the development of leaves (Coley & Barone, ; Koricheva & Barton, ; Wiggins et al , ; Barton et al , ) and during the whole ontogeny of individuals (Boege & Marquis, ; Barton & Koricheva, ), the study of natural selection on such traits has mostly focused on single points across the lifetime of individuals (Barton & Boege, ; but see Cope et al , ), usually controlling for leaf age (Mauricio & Rausher, ; Tiffin & Rausher, ; Agrawal et al , ). A few reports suggest, however, that the intensity of natural selection can change across plant ontogeny (Tiffin, ; Gómez, ), promoting ontogenetic trajectories of ecophysiological (Maherali et al , ) and defensive traits (Cope et al , ).…”

“…Because herbivore pressure can be variable along plant development (Hanley et al , ; Fenner et al , ; Warner & Cushman, ; Quintero et al , ), it can act as a selective force favoring the expression of greater values of defensive traits at the most vulnerable plant ontogenetic stages (Agrawal et al , ; Barton & Boege, ). For example, a recent study shows that the adaptive value of salicinoid phenolic glycosides changes during the ontogeny of Populus tremuloides (Cope et al , ). The benefit of particular defensive traits is likely to change during plant development as a function of the physiological priorities of different plant stages (Herms & Mattson, ), the fitness value of different organs (Boege & Marquis, ; Barton & Koricheva, ; Villamil, ), their efficiency deterring specific herbivores (Van Bael et al , ; Boege, ; Boege & Marquis, ) and/or as a result of ontogenetic niche changes derived from the interaction with different species (Perez & Munch, ; Fonseca‐Romero et al , ; Villamil et al , ).…”

Trait plasticity and trade‐offs shape intra‐specific variation in competitive response in a foundation tree species

“…The negative covariance between competitive response and foliar salicin production is consistent with a genotypic growth-defense trade-off. Aspen defense compounds are known to covary negatively with growth rate among genotypes, although the magnitude of that trade-off varies with nutrient availability, sex, and developmental stage (Osier & Lindroth, 2006;Cope et al, 2019;Fig. 3 Relationships between genotype-mean trait responses and genotype-mean competitive response in Populus tremuloides.…”

“…Alternatively, genotypic variation in competitive response may attenuate over time, especially if alternative stressors such as herbivore outbreaks come into play. Production of secondary metabolites changes throughout development in aspen; such changes are nonlinear and show significant variation among genotypes (Cope et al ., 2019). Therefore, differential competitive ability among genotypes based on their defense trait expression as juveniles may shape the phenotypic composition of populations at future developmental stages in unexpected ways.…”

Predictability of Biotic Stress Structures Plant Defence Evolution

“…These trajectories can have significant genetic variation and/or be phenotypically variable within populations, influenced by plastic responses to different stressors. Thus, natural selection should favour plants allocating resources to specific defensive traits only when most needed or when other functions with a greater impact on fitness are not compromised [51,52]. The genes underlying these allocation trade-offs, such as those between defence and growth, are now being identified [53,54].…”