Evolutionary history predicts plant defense against an invasive pest

Abstract

It has long been hypothesized that invasive pests may be facilitated by the evolutionary naïveté of their new hosts, but this prediction has never been examined in a phylogenetic framework. To address the hypothesis, we have been studying the invasive viburnum leaf beetle (Pyrrhalta viburni), which is decimating North American native species of Viburnum, a clade of worldwide importance as understory shrubs and ornamentals. In a phylogenetic field experiment using 16 species of Viburnum, we show that old-world Viburnum species that evolved in the presence of Pyrrhalta beetles mount a massive defensive wound response that crushes eggs of the pest insect; in contrast, naïve North American species that share no evolutionary history with Pyrrhalta beetles show a markedly lower response. This convergent continental difference in the defensive response of Viburnum spp. against insect oviposition contrasts with little difference in the quality of leaves for beetle larvae. Females show strong oviposition preferences that correspond with larval performance regardless of continental origin, which has facilitated colonization of susceptible North American species. Thus, although much attention has been paid to escape from enemies as a factor in the establishment and spread of nonnative organisms, the colonization of undefended resources seems to play a major role in the success of invasive species such as the viburnum leaf beetle.defense-free space | invasion ecology | phylogenetic ecology | preference-performance relationship T he establishment and spread of nonnative pests in novel environments has often been viewed as a result of escape from natural enemies present in the native range (1-3), and this topdown view is supported by the success of classical biological control programs against a number of invasive pests (4-6). Nonetheless, there is growing evidence that a lack of defenses in evolutionarily naïve hosts creates opportunities for exotic pests (7-10). For example, because herbivores are potent agents of natural selection for plant defense (11)(12)(13)(14), evolutionarily naïve plants may be particularly susceptible to invasive pest insects. Previous observations of island floras have indicated low defense and high susceptibility of naïve plants (15, 16), but this pattern has not been rigorously examined in an evolutionary framework. In particular, this bottomup notion emphasizes past evolutionary ecology of plant-herbivore interactions as being critical for community stability.We tested the hypothesis that a lack of shared evolutionary history between plants and herbivores creates defense-free space, facilitating pest invasions. In a phylogenetically controlled field experiment with 16 species of North American and Eurasian Viburnum spp. (Adoxaceae, Dipsacales) (Fig. 1), we tested for the impact of plant continental origin, a proxy for shared evolutionary history with specific herbivores, on defense against the Eurasian Pyrrhalta viburni, an emerging invasive pest in North America. Theory predicts that plant defe...

Oviposition strategy as a means of local adaptation to plant defence in native and invasive populations of the viburnum leaf beetle

“…The main benefit of this behaviour is thought to be overcoming a specific type of plant defence: the production of wound tissue crushing or expelling eggs outside the egg cavity in the weeks following oviposition (figure 1b). Egg survivorship was seven times lower on twigs expressing such wound response, and it was negatively correlated with intensity of infestation (number of egg masses per twig) on several Viburnum hosts including V. opulus [18,22]. Twigs heavily infested with egg masses often die, circumventing their ability to produce wound tissue.…”

“…On the other hand, the exceptional defensive capacity of V. tinus may also originate from the specific environmental conditions inherent to the Tinus site. Although there is evidence that the defensive patterns observed are consistent between gardens for V. opulus [18,22] and V. tinus (G. A. Desurmont 2005, unpublished data), repeating studies of these plant defences in common gardens would distinguish between the genetic basis and the influence of environmental factors on the woundresponse capacity of the hosts. In addition, testing the behaviour of Tinus and Opulus beetles on plants from both hosts grown in reciprocal common gardens would help determine whether environmental conditions may influence oviposition behaviour via modification of host traits.…”

“…have been shown to be generally lower than Eurasian spp. [22]. We speculate that the combination of an effective 'offensive' behaviour, coupled with a generalized pattern of lower defences in novel hosts, provided a coevolutionary mismatch favouring VLB in its introduced range and facilitating a devastating invasion.…”

“…whose defences have been evaluated, enhanced defensive response to increased oviposition appears to be uniquely displayed by V. tinus [22], and is associated with increased tolerance to oviposition (i.e. negligible twig mortality caused by oviposition; figure 2b).…”

The sudden emergence of pathogenicity in insect–fungus symbioses threatens naive forest ecosystems

“…We propose that the shift is not a consequence of a change in the insect behaviour, or a novel host association, though these may occur. It may instead be a new expression of 'old' behaviours in a new ecological context, in other words an evolutionary mismatch [54].…”