Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

Kessler, André; Halitschke, Rayko

doi:10.1111/j.1365-2435.2009.01639.x

Cited by 223 publications

(295 citation statements)

References 117 publications

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“…Alternatively, there may exist indirect interactions among herbivores, plants, and pollinators that may collectively favor the evolution of greater inducibility in inbreeding taxa. Herbivory can alter floral phenotypes and influence pollinators (31,43,44), and the induction of deterrent or toxic metabolites in reward tissues such as pollen and nectar could be disproportionately costly to obligately outcrossing, compared with inbreeding, taxa (45). Because of the ancestral nature of SI in this family, a hypothesis of repeated herbivore-mediated shifts in both defense strategy and mating system seems less likely, although we note that our data cannot unequivocally exclude this possibility.…”

Section: Resultscontrasting

confidence: 40%

Plant mating system transitions drive the macroevolution of defense strategies

Campbell

Kessler

2013

Proc. Natl. Acad. Sci. U.S.A.

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Understanding the factors that shape macroevolutionary patterns in functional traits is a central goal of evolutionary biology. Alternative strategies of sexual reproduction (inbreeding vs. outcrossing) have divergent effects on population genetic structure and could thereby broadly influence trait evolution. However, the broader evolutionary consequences of mating system transitions remain poorly understood, with the exception of traits related to reproduction itself (e.g., pollination). Across a phylogeny of 56 wild species of Solanaceae (nightshades), we show here that the repeated, unidirectional transition from ancestral self-incompatibility (obligate outcrossing) to self-compatibility (increased inbreeding) leads to the evolution of an inducible (vs. constitutive) strategy of plant resistance to herbivores. We demonstrate that inducible and constitutive defense strategies represent evolutionary alternatives and that the magnitude of the resulting macroevolutionary tradeoff is dependent on the mating system. Loss of self-incompatibility is also associated with the evolution of increased specificity in induced plant resistance. We conclude that the evolution of sexual reproductive variation may have profound effects on plant-herbivore interactions, suggesting a new hypothesis for the evolution of two primary strategies of plant defense.herbivory | induced resistance | coevolution | plant defense theory | Solanum

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Section: Resultscontrasting

confidence: 40%

Plant mating system transitions drive the macroevolution of defense strategies

Campbell

Kessler

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Herbivory may change other floral traits that influence pollinator attraction and behavior. Recent experiments have shown that floral volatile blends can change following herbivore damage (Theis et al 2009), sometimes with consequences for pollinator behavior (Kessler and Halitschke 2009). However, timing of damage may be critical (Effmert et al 2008), and we found no effect of herbivory on floral volatiles.…”

Section: Indirect Effects On Mutualistscontrasting

confidence: 35%

Herbivory reduces plant interactions with above‐ and belowground antagonists and mutualists

Barber

Adler

Theis

et al. 2012

Ecology

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Abstract. Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.

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“…Herbivore feeding guilds have been found to differ in their effect on flower visitors (Rusman et al 2018), and dual infestation of herbivores on the leaves may potentially further modulate these effects. Leaf-feeding herbivores may thereby strongly affect plant reproductive success when they affect arrival of herbivores that feed on flowers or seed pods (McArt et al 2013) or interactions with pollinators (Kessler and Halitschke 2009, Lucas-Barbosa et al 2011. In our study, we found that the impact on seed set was not significant and dependent on the plant population.…”

Section: Discussionmentioning

confidence: 50%

“…This could be explained by different processes that are non-exclusive: 1) the physical movement of insects from leaves towards flowers as the season progressed, 2) systemic induction of phenotypic changes i.e. leaf herbivory causes phenotypic changes in the reproductive parts (McCall and Irwin 2006, Kessler and Halitschke 2009, Lucas-Barbosa et al 2011, or 3) effects of induced plant phenotypic changes cascaded via consecutive community members up to species that are associated with flowers in a spatial-temporal manner (Utsumi et al 2010). Herbivore feeding guilds have been found to differ in their effect on flower visitors (Rusman et al 2018), and dual infestation of herbivores on the leaves may potentially further modulate these effects.…”

Section: Discussionmentioning

confidence: 99%

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

Stam

Dicke

Poelman

2018

Oikos

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In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear. Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production. Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited. Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences.

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Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

Cited by 223 publications

References 117 publications

Plant mating system transitions drive the macroevolution of defense strategies

Plant mating system transitions drive the macroevolution of defense strategies

Herbivory reduces plant interactions with above‐ and belowground antagonists and mutualists

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

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