Reassociation of an invasive plant with its specialist herbivore provides a test of the shifting defence hypothesis

Abstract

The shifting defence hypothesis (SDH) predicts that after invasive plants are introduced to new ranges, they will evolve reduced resistance to specialist herbivores and increased resistance to generalist herbivores because they can escape from specialists but are still attacked by generalists in their nonnative ranges. For this to be true, the subsequent introduction of native specialist herbivores should reverse the above evolutionary processes, but evidence collected so far is scarce. Here, we address this research gap by comparing resistance to specialist and generalist herbivores and resistance‐related traits in the invasive plant Ambrosia artemisiifolia from five populations with about a decade history of infestation by the accidentally introduced native specialist leaf beetle Ophraella communa (infested populations), and three populations without such infestation history (uninfested populations). In common garden experiments, the specialist O. communa performed better on uninfested populations than on infested populations, whereas two generalist insects, Spodoptera litura and Helicoverpa armigera, performed better on infested populations. Chemical analyses showed that plants from infested populations had lower concentrations of chlorogenic acid, an antigeneralist secondary compound that can attract O. communa. Furthermore, across mother plants from all populations studied, chlorogenic acid content was negatively correlated with larval growth of S. litura and positively correlated with that of O. communa. Finally, quantitative defence traits did not differ between infested and uninfested populations. Although our results are most consistent with rapid evolution caused by enemy reassociation, we cannot exclude the possibility that observed differences in resistance result from multiple introductions or selections from other environmental factors. Synthesis. These results suggest that reassociation with a specialist herbivore from the native range may result in a rapid evolution of increased resistance to specialist herbivores and reduced resistance to generalist herbivores in the introduced range, which is likely to be mediated by the reduced production of secondary chemicals that can deter generalists while attracting the introduced specialist. This study supports the shifting defence hypothesis (SDH) from a new viewpoint, emphasizing the importance of incorporating the impacts of both specialist and generalist herbivores when evaluating the long‐term control effects of classical biological control programmes.

Rapid evolution of invasive traits facilitates the invasion of common ragweed, Ambrosia artemisiifolia

“…This would indicate that such a trade‐off leading to lower competitive ability under biological control management has evolved after only one to two decades (i.e., selection on the total biomass: Q SC‐h > F SC‐h ), but additional bioassays are needed to substantiate such trade‐offs. A very recent study found a higher defence level in O. communa ‐infested A. artemisiifolia populations than uninfested populations in China (Wan, Huang, Yu, & Peng, ), which is well in line with our findings. Our study does support the EICA hypothesis associated with invasion success (Blossey & Nötzold, ; Bossdorf, ), however, the results also show that the initially evolved increased competitive ability after the introduction into a new region can also be lost again quickly with the re‐association of enemies, in this case specialize herbivores introduced for biological control (Joshi & Vrieling, ; Müller‐Schärer et al, ).…”

Comparison of chrysanthemum flowers grown under hydroponic and soil-based systems: yield and transcriptome analysis

“…Chlorogenic acid was measured according to the methods described by Jinlong Wan (2019) [ 85 ]. A total of 0.05 g of powered sample was immersed in 5 mL of methanol-0.4% phosphoric acid solution.…”

“…Two solvent systems of the mobile phase: solvent A, acetonitrile/0.4% phosphoric acid (10:90, v:v); solvent B, 100% acetonitrile. The HPLC operating procedures was the same as that described in Jinlong Wan (2019) [ 85 ]. Chlorogenic acid concentrations of samples were calculated in relation to standard curves generated with relevant standards.…”

Is biocontrol efficacy rather driven by the plant or the antagonist genotypes? A conceptual bioassay approach

“…This result could be due to the shorter generation time of the antagonist as compared to its host plant, leading to a more virulent antagonist genotype (Kaltz et al 1999), or due to its oligophagous nature, which allows Ophraella to deal with a large diversity of plant defense chemicals (Ali and Agrawal 2012). The fact that the Ambrosia genotype only differed for total leaf area consumed by the larvae, but did not influence survival and developmental time, or the weight of the herbivore, may indicate that Ophraella can compensate for observed differences in secondary plant metabolites in Ambrosia (Fukano and Yahara 2012;Sun and Roderick 2019;Wan et al 2019) by adapting their feeding rate (Müller et al 2006). Significant Ambrosia-Ophraella G × G interactions were found only for two out of 13 variates measured, i.e., L2 survival and dry weight of adults.…”