The Role of Herbivores in the Maintenance of a Flower Color Polymorphism in Wild Radish

Abstract

Plant species exhibiting polymorphisms with respect to flower color are widespread. Our understanding of the selection pressures that may maintain these color polymorphisms has primarily been confined to one set of organisms—pollinators. Yet, selection on flower color may also be driven by other agents, such as herbivores, especially in cases where pollinators and herbivores are using the same or correlated traits to select plants. A wealth of studies have documented pollinator preference for anthocyanin‐recessive color morphs (A−; yellow and white flowers) of wild radish, Raphanus sativus, over anthocyanin‐dominant morphs (A+; pink and bronze flowers); yet, differences in pollination alone do not explain the maintenance of the flower color polymorphism. Here, we ask whether variation in flower color in R. sativus influences the preference and performance of herbivores for A− flower color morphs vs. A+ flower color morphs in four types of herbivores (generalist and specialist Lepidoptera, slugs, aphids, and thrips). We found that all herbivores except for aphids and thrips preferred flowering A− color morphs compared to A+ morphs of R. sativus. Furthermore, all herbivores except larvae of specialist and generalist Lepidoptera performed better on A− color morphs. Differences in plant secondary chemistry may play a role in differential herbivore preference and performance on the anthocyanin flower color morphs. Chemical analyses of leaf secondary compounds (indole glucosinolates) revealed that A+ color morphs produced higher concentrations of indole glucosinolates than A− morphs in the presence of herbivore damage. Therefore, herbivores may exhibit lower preference for A+ color morphs, and these morphs may support lower herbivore performance because they are heavily defended once damaged. This is the first study, to our knowledge, to document differential preference and performance of herbivores for different flower color morphs. Previous studies have shown that increased herbivore damage can have profound negative direct and indirect effects on the reproduction of R. sativus. The data presented here suggest that differential preference and performance of herbivores for R. sativus color morphs may counter selection on flower color exerted by pollinators.

Development of an Insect Herbivore and its Pupal Parasitoid Reflect Differences in Direct Plant Defense

“…High concentrations of neoglucobrassicin in plants from the Kimmeridge and Winspit populations corresponded to reduced biomass and prolonged development of the herbivore when reared on these two populations. Indole glucosinolates are known to be induced by herbivory and fungal infection and to affect the growth and development of insect herbivores deleteriously (Rostás et al 2002;Irwin et al 2003). Levels of primary metabolites, such as nitrogen and amino acids, were not measured in this study.…”

How plant?animal interactions signal new insights in communication

“…Anthocyanin-recessive flowers suffer more herbivore damage than do the anthocyanin-dominant flowers because the latter are more strongly defended by secondary compounds such as glucosinolates. The diverging selection pressures of pollinators and herbivores result in an evolutionary stable flower colour polymorphism [23]. A similar influence of multiple receivers on signal design occurs in the Andean monkeyflower Mimulus luteus, where selection for nectar guides exerted by insect pollinators and by hummingbirds probably leads to the disruptive selection of nectar guide size and shape [24].…”

“…We argue that the evolution of signals is best understood by considering all receivers, especially those with disparate ecologies. Selection pressures by different receivers might result in directional as well as disruptive signal evolution [23,24]. In the wild radish Raphanus sativus, pollinators prefer anthocyanin-recessive white floral colour morphs, but frequencies of anthocyanin-dominant pink morphs remain constant over time.…”

“…In this respect, the classic idea of disperser and pollination syndromes might be outdated. Such syndromes might not be targeted solely at mutualists (as traditionally assumed), but might also be aimed at avoiding antagonists [23]. The most obvious example are UV-reflecting floral pigments (de-aromatized isoprenylated phloroglucinols), which are used to attract mutualists, but which also function simultaneously as chemical defence against herbivores (Figure 1d,e) [33].…”

Attracting Antagonists: Does Floral Nectar Increase Leaf Herbivory?

“…For example, in Ipomoea purpurea, the compounds responsible for flower color and for chemical defenses against herbivores are produced by a shared biosynthetic pathway, so that floral morph is related to leaf herbivore survival (Simms andBucher 1996, Fineblum andRausher 1997). Preferences of a diversity of herbivores (Irwin et al 2003) and pollinators (Stanton et al 1989) also vary with color morphs of Raphanus raphanistrum. Chemical defenses in petals are higher than in leaves and vary between color morphs, suggesting that the mechanism for differential herbivore resistance between morphs is linked to these defenses (Strauss et al 2004).…”