Evolution of plant defences along an invasion chronosequence: defence is lost due to enemy release – but not forever

Abstract

Summary1. The success of invasive plants has often been attributed to their rapid evolution at the introduced range. In particular, release from native enemies has been suggested to select for an evolutionary shift in resource allocation patterns from herbivore defence to increased size. Such evolutionary processes can take place not only between the native and invasive ranges but also within the invasive range over time, but this premise has been very seldom studied. 2. In this study, we examined the potential for post-invasion evolution in two traits hypothesized to facilitate plant invasion success, that is herbivore resistance and allelopathic ability. We studied these traits in the invasive plant Impatiens glandulifera by comparing plants from its native populations and from populations across its invasion chronosequence. 3. Results of common-garden experiment and chemical analyses revealed that plants from native populations or older populations within the invasive range show greater resistance to the generalist herbivore, Deilephila elpenor, coupled with greater production of the secondary defence compound 2-methoxy-1,4-naphthoquinone glycoside. In contrast, no differences were found between populations in their allelopathic effect on the germination of the co-occurring neighbour, Urtica doica. Finally, results from a field survey suggested that older populations within the invasive range incur greater attack rates from local herbivores compared to more recently established populations. 4. Synthesis. Our findings support the idea that the selection pressure of enemy release at the introduced range might attenuate over time, leading to the evolutionary recovery of enemy resistance. This study emphasizes the importance of incorporating the effect of time since introduction when examining evolutionary or ecological processes of plant invasions.

Do local enemies attack alien and native Impatiens alike?

“…Taking into account our results and those from Switzerland, we can speculate that, since I. glandulifera had become acclimated to higher pressure in its primary area of occurrence, its success was driven not only by release from enemies but also by higher tolerance of the negative effects of their presence, which would be consistent with the assumptions by Schierenbeck et al [79] and the enemy tolerance hypothesis [80]. In line with this, Gruntman et al [44] found that herbivore pressure on I. glandulifera in the introduced range increased with age of populations, with the highest levels noted for those 45-65 years old. However, herbivore pressure for the oldest populations (65-85 years) sharply fell to the lowest level, equal to the level noted for native populations.…”

“…Gruntman et al [44] showed that the post-introduction herbivore resistance of I. glandulifera rises with time, while its allelopathic effects do not. They further stressed the need for more investigation, citing their earlier finding that the allelopathic ability of the species significantly evolved in the invaded range.…”

“…For the tests, we used the alien Impatiens glandulifera and I. parviflora, and the native I. noli-tangere. Despite the very high invasiveness of both alien species [41], they have not been subjected to such tests in Poland at all, and rarely elsewhere in Europe [42][43][44]; this is surprising in view of the efforts made to develop biological control methods against these plants [45,46].…”

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

“…Therefore, geographic variation in various environmental factors along latitude (north vs. south) seem to be insufficient to explain all observed patterns. Finally, because all of the plants examined in the present study were grown from first‐generation seeds, the influence of maternal effects cannot be completely ruled out (Agrawal et al, ; Gruntman, Segev, Glauser, & Tielbörger, ). Nevertheless, we argue that maternal effects are an unlikely explanation because such effects on plant defence are typically short‐lived, functioning very early in the development of progeny (Agrawal, ; Didiano et al, ; Stanton, ; Turley et al, ), and thus are not expected to persist throughout the course of the about 9‐week common garden experiments conducted in our study.…”

Contrasting effects of specialist and generalist herbivores on resistance evolution in invasive plants

“…, Gruntman et al. ), an evolutionary shift in resistance could help alien plants to become invasive when it helps them overcome biotic resistance from newly encountered generalists. In apparent contrast to our finding, another recent meta‐analysis by Felker‐Quinn et al.…”