The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca

Hochwender, Cris G.; Marquis, Robert J.; Stowe, Kirk A.

doi:10.1007/s004420050042

Cited by 118 publications

(114 citation statements)

References 71 publications

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“…First, early models and intraspecific data from A. syriaca suggested that regrowth may be predicted by the rootto-shoot ratio, whereby those species that invest relatively more underground will be able to better recover from aboveground damage (3,24). Indeed, we found that root-to-shoot ratio was a good predictor of regrowth, but that the association between high investment in roots and ability to regrow after damage was phylogenetically constrained (rc: r ϭ 0.387, P ϭ 0.022, pic: P ϭ 0.841).…”

Section: Resultsmentioning

confidence: 99%

Phylogenetic escalation and decline of plant defense strategies

Agrawal

Fishbein

2008

Proc. Natl. Acad. Sci. U.S.A.

167

194

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As the basal resource in most food webs, plants have evolved myriad strategies to battle consumption by herbivores. Over the past 50 years, plant defense theories have been formulated to explain the remarkable variation in abundance, distribution, and diversity of secondary chemistry and other defensive traits. For example, classic theories of enemy-driven evolutionary dynamics have hypothesized that defensive traits escalate through the diversification process. Despite the fact that macroevolutionary patterns are an explicit part of defense theories, phylogenetic analyses have not been previously attempted to disentangle specific predictions concerning (i) investment in resistance traits, (ii) recovery after damage, and (iii) plant growth rate. We constructed a molecular phylogeny of 38 species of milkweed and tested four major predictions of defense theory using maximum-likelihood methods. We did not find support for the growth-rate hypothesis. Our key finding was a pattern of phyletic decline in the three most potent resistance traits (cardenolides, latex, and trichomes) and an escalation of regrowth ability. Our neontological approach complements more common paleontological approaches to discover directional trends in the evolution of life and points to the importance of natural enemies in the macroevolution of species. The finding of macroevolutionary escalating regowth ability and declining resistance provides a window into the ongoing coevolutionary dynamics between plants and herbivores and suggests a revision of classic plant defense theory. Where plants are primarily consumed by specialist herbivores, regrowth (or tolerance) may be favored over resistance traits during the diversification process.cardenolides ͉ coevolution ͉ macroevolutionary trends ͉ milkweed Asclepias ͉ plant defense theory M ilkweeds (Asclepias spp., Apocynaceae) are prime candidates for a clade-based approach to testing plant defense theories because of their well known defensive strategies and tremendous variation in expression of these traits (1-3). Three traits-cardenolides, latex, and trichomes-have been strongly implicated in providing milkweed resistance against herbivores. Each of these traits has been demonstrated to quantitatively affect the behavior (4, 5), performance (1, 6, 7), and abundance (8) of herbivores in the field. The resistance provided by these three traits occurs despite the fact that most milkweed herbivores are specialists and have adaptations to cope with each defense (4, 5, 9). Our central goal was thus to evaluate what factors predict variation in defense investment across the clade.We tested four major predictions of classic plant defense theory using phylogenetically explicit analyses employing maximum-likelihood estimation of defense trait evolution (10, 11). First, do the individual resistance traits used by plants trade off due to redundancy, or do they repeatedly evolve together as a suite of covarying traits (12, 13)? Second, does plant growth rate covary with investment in resistance traits as p...

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Section: Resultsmentioning

confidence: 99%

Phylogenetic escalation and decline of plant defense strategies

Agrawal

Fishbein

2008

Proc. Natl. Acad. Sci. U.S.A.

167

194

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“…Four hypotheses could explain the lack of an interaction between competition and herbivory in C. vulgare performance. First, there may be no tradeoff in resource allocation for growth versus defense or tolerance of herbivory for C. vulgare in its final, flowering year, in contrast to other studies (e.g., Simms 1992; Strauss and Agrawal 1999;Hochwender et al 2000;Stowe et al 2000). If rosettes in their flowering year have large amounts of stored nutrients in their taproots, then allocation of resources to both growth and defense or tolerance may be possible.…”

Section: Interaction Of Competition and Herbivorymentioning

confidence: 92%

No interaction between competition and herbivory in limiting introduced Cirsium vulgare rosette growth and reproduction

2009

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Both competition and herbivory have been shown to reduce plant survival, growth, and reproduction. Much less is known about whether competition and herbivory interact in determining plant performance, especially for introduced, weedy plant species in the invaded habitat. We simultaneously evaluated both the main and interactive effects of plant neighbors and insect herbivory on rosette growth and seed reproduction in the year of flowering for Cirsium vulgare (bull thistle, spear thistle), an introduced Eurasian species, in tallgrass prairie in 2 years. Effects of insect herbivory were strong and consistent in both years, causing reduced plant growth and seed production, whereas the effects of competition with established vegetation were weak. The amount of herbivore damage inflicted on rosettes did not depend on the presence of neighbor plants. We also found no interaction between competition and herbivory on key parameters of plant growth and fitness. The results of this study contradict the hypothesis that competitive context interacts with insect herbivory in limiting the invasiveness of this introduced thistle. Further, the results provide additional, experimental evidence that high levels of herbivory on established rosettes by native insects exert significant biotic resistance to the invasiveness of C. vulgare in western tallgrass prairie.

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“…However, it would seem that stored resources cannot be solely responsible for compensatory ability because presumably those resources would have been used for some fitness enhancing function regardless of damage. Instead, it is possible that the pattern of resource allocation (e.g., Hochwender et al 2000) or the timing of damage relative to the allocation of resources could affect compensatory ability. In addition, the specific pattern of resource allocation might differ in damaged and undamaged plants.…”

Section: Introductionmentioning

confidence: 99%

Compensation for Herbivory in Wild Sunflower: Response to Simulated Damage by the Head-Clipping Weevil

Pilson

Decker

2002

Ecology

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Abstract. Herbivore damage is generally detrimental to plant fitness, and the evolutionary response of plant populations to damage can involve either increased resistance or increased tolerance. While characters that contribute to resistance, such as secondary chemicals and trichomes, are relatively well understood, characters that contribute to a plant's ability to tolerate damage have received much less attention. Using Helianthus annuus (wild sunflower) and simulated damage of Haplorhynchites aeneus (head-clipping weevil) as a model system, we examined morphological characters and developmental processes that contribute to compensatory ability. We performed a factorial experiment that included three levels of damage (none, the first two, or the first four inflorescences were clipped with scissors) and eight sires each mated to four dams. We found that plants compensated fully for simulated head-clipper damage and that there was no variation among plant families in compensatory ability: seed production and mean seed mass did not vary among treatments, and sire ϫ treatment interactions were not significant. Plants used four mechanisms to compensate for damage: (1) Clipped plants produced significantly more inflorescences than unclipped plants. Plants produced these additional inflorescences on higher order branches at the end of the flowering season. (2) Clipped plants filled significantly more seeds in their remaining heads than did unclipped plants. (3) Clipped plants, because they effectively flowered later than unclipped plants, were less susceptible to damage by seedfeeding herbivores other than Haplorhynchites. (4) In later heads, seed size was greater on clipped plants, which allowed mean seed size to be maintained in clipped plants. Although there was genetic variation among the families used in this experiment for most of the characters associated with compensation for damage (seed number, mean seed size, mean flowering date, length of the flowering period, and branching morphology), in analyses of these characters, no sire ϫ treatment interactions were significant indicating that all of the families relied on similar mechanisms to compensate for damage.

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The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca

Cited by 118 publications

References 71 publications

Phylogenetic escalation and decline of plant defense strategies

Phylogenetic escalation and decline of plant defense strategies

No interaction between competition and herbivory in limiting introduced Cirsium vulgare rosette growth and reproduction

Compensation for Herbivory in Wild Sunflower: Response to Simulated Damage by the Head-Clipping Weevil

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