Trade-offs constrain the evolution of an inducible defense within but not between plant species
- PMID: 31365759
- DOI: 10.1002/ecy.2857
Trade-offs constrain the evolution of an inducible defense within but not between plant species
Abstract
Inducible defense is a common form of phenotypic plasticity, and inducibility (change in defense after herbivore attack) has long been predicted to trade off with constitutive (or baseline) defense to manage resource allocation. Although such trade-offs likely constrain evolution within species, the extent to which they influence divergence among species is unresolved. We studied cardenolide toxins among genetic families in eight North American Asclepias species, spanning the full range of defense in the genus. Using common environment experiments and chemical assays, we report a consistent trade-off (negative genetic correlation) between concentrations of constitutive cardenolides and their inducibility within each species. However, no trade-off was found in a phylogenetic analysis across species. To investigate factors driving differences in defense allocation among species we used latitude as a proxy for growing season and herbivore pressure and found that divergence into lower latitudes resulted in evolution of higher cardenolides overall. Next we used an enzymatic assay of the cellular target of cardenolides (sodium-potassium ATPase) and confirm that higher cardenolides resulted in stronger toxicity to a sensitive species, but not to specialized monarch butterflies. Thus, plant speciation into biogeographic regions with alternative resources or pest pressure resulted in the macroevolution of cardenolide defense, especially against unspecialized herbivores. Nonetheless, trade-offs persist in the extent to which this defense is allocated constitutively or is inducible among genotypes within each species.
Keywords: cardenolide cardiac glycoside; chemical ecology; milkweed Asclepias; monarch butterfly Danaus plexippus; phenotypic plasticity; plant defense theory; trade-offs.
© 2019 by the Ecological Society of America.
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References
Literature Cited
-
- Adler, F. R., and R. Karban. 1994. Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. American Naturalist 144:813-832.
-
- Agrawal, A. A. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research 7:651-667.
-
- Agrawal, A. A. 2007. Macroevolution of plant defense strategies. Trends in Ecology and Evolution 22:103-109.
-
- Agrawal, A. A. 2011. Current trends in the evolutionary ecology of plant defence. Functional Ecology 25:420-432.
-
- Agrawal, A. A., and M. Fishbein. 2006. Plant defense syndromes. Ecology 87:S132-S149.