A major constraint on the evolution of plant defense against herbivores may be the non-independent expression of traits that mediate resistance. Since plant tissues are often targeted by distinct herbivores, we hypothesize that natural selection for differential defense across plant parts may only be realized when traits are not genetically correlated. Strong differences in herbivore pressure from the insect community may therefore cause genetic correlations among defense traits differ not only among tissues, but also between populations within a species even in spite of gene flow. We quantified cardenolide defenses by HPLC in roots, leaves and seed tissue of two nearby common milkweed (Asclepias syriaca) populations to investigate 1) whether cardenolide chemistry differs between tissues and populations using PCA and nMDS, 2) to what extent genetic correlations (i.e. family means) among defense traits are tissue- and toxin-specific, and 3) whether tissue-specific differences in the cardenolide chemistry between populations may be a result of heterogeneous selection by performing univariate and multivariate QST-FST analysis.
Results/Conclusions
We report that roots, leaves and seeds of common milkweed (Asclepias syriaca) strongly varied in their multivariate concentration and composition of 28 cardenolide toxins, with seeds and roots showing the greatest difference between two nearby ( < 1 km) populations. Genetic correlations between specific toxins within tissues were minimal in roots and leaves and more evident in seeds overall, and genetic correlations between tissues for each toxin were population-specific and more evident for polar (less toxic) rather than non-polar cardenolides (more toxic). These differences mirrored signatures of divergent selection between populations (QST > FST), measured by multivariate and univariate QST–FST comparisons. A nitrogen-containing and highly toxic non-polar cardenolide, labriformin, stood out for being under strong divergent selection at the whole plant level, but not among individual tissues. This suggests that cardenolides highly toxic against most attackers are not evolutionarily constrained to tissue-specific expression compared to other, less toxic compounds.
