Resistance and tolerance to herbivory in <i>Solidago altissima</i> (Asteraceae): Genetic variability, costs, and selection for multiple traits

Hakes, Alyssa S.; Cronin, James T.

doi:10.3732/ajb.1000485

Cited by 27 publications

(34 citation statements)

References 80 publications

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“…Various greenhouse and common-garden studies have revealed considerable genotypic variability in goldenrod resistance to insect herbivore attack (e.g., Maddox and Root 1987, McCrea and Abrahamson 1987. In the common-garden experiment, we did not find a signifi-cant effect of population of origin on genet resistance levels (Hakes and Cronin 2011b); however, we cannot reject the possibility that carryover effects within source populations inflated the variability seen among genets in resistance levels, and were subsequently lost in the present experiment. Of the 103 goldenrod genotypes used in the common-garden study, the 14 most different were used in this study.…”

Section: Discussioncontrasting

confidence: 69%

Successional changes in plant resistance and tolerance to herbivory

Hakes

Cronin

2012

Ecology

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Despite considerable research on plant defenses, we know very little about how temporal changes in the environment may influence resistance and tolerance levels, or the costs and benefits of these defense strategies for long-lived plant species. We hypothesized that, in successional habitats, predictable environmental changes should favor strong plasticity in defense phenotypes and that the costs, benefits, and levels of tolerance and resistance will change with environmental context. Using a widely distributed, old-field perennial, late goldenrod (Solidago altissima), we conducted a field experiment to test these predictions. We planted goldenrod genets exhibiting varying levels of resistance and tolerance into three early-successional and three late-successional fields (approximately three and 15 years in age, respectively) and experimentally measured resistance and tolerance levels and their associated costs and selection coefficients. We found a significant effect of successional stage but no effect of genotype or stage-genotype interaction on defense levels. Genets planted in early-successional fields appeared to be more resistant and less tolerant to herbivory than those same genets planted in late-successional fields. There were significant trade-offs between resistance and tolerance in early-successional fields but not in late-successional fields. Each late-successional field exhibited a significant cost or selection gradient for resistance, but there was no general pattern of resistance costs or selection gradients specific to a successional stage class. In contrast, there was evidence of stage-specific costs of tolerance; late-successional fields exhibited significant costs of tolerance whereas early-successional fields did not. There was no evidence of direct selection for or against tolerance in either stage. Our results suggest that defense phenotypes might change in qualitative ways during succession. High resistance in early stages may be attributed to associational effects of the early-successional community, reducing the probability of damage, and despite a cost of tolerance in late stages, tolerance may be beneficial in mitigating the effects of both herbivory and environmental stresses (i.e., low light availability) that limit fitness in these fields. This study provides experimental evidence that succession can strongly influence defense phenotypes and promote temporal variability in relative resistance and tolerance levels.

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Section: Discussioncontrasting

confidence: 69%

Successional changes in plant resistance and tolerance to herbivory

Hakes

Cronin

2012

Ecology

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“…It is even possible that low attack rates on S. gigantea reflect the evolution of increased resistance after G. gallaesolidaginis's host shift-and if resistance and tolerance trade off (Fornoni et al 2004;Núñez-Farfán et al 2007;Agrawal 2011; but see Jokela et al 2000) then a response to selection in resistance might pre-empt a response in tolerance. We have not measured resistance to G. gallaesolidaginis by S. altissima/gigantea, although Hakes and Cronin (2011) found selection against resistance to leaf-chewing herbivores in S. altissima (and no evidence for resistance-tolerance tradeoffs). Finally, the strength of selection on G. gallaesolidaginis virulence will depend on how much its impact on Solidago is mediated by its sequestration of plant resources into gall and insect tissues, versus by incidental damage to young leaves, meristems, and vascular tissue during gall formation.…”

Section: Discussionmentioning

confidence: 73%

“…Hakes and Cronin (2011) detected significant selection on S. altissima for increased tolerance to leaf-chewing herbivores, but measured very low heritability for tolerance and suggested this as a constraint on the evolution of tolerance. It is, however, unknown how tolerance of leaf-chewing relates to tolerance of gallmaking.…”

Section: Discussionmentioning

confidence: 91%

“…The greater impact of G. gallaesolidaginis on S. altissima is consistent with predictions based on the expected evolution of higher tolerance (by the host plant) and of lower virulence (by the attacking insect) in the older association. The Gnorimoschema-Solidago system is one in which these expectations are particularly clear: there is little evidence for costs of tolerance in S. altissima (Hakes and Cronin 2011), and as a host-specialist, solitary, internally feeding herbivore Gnorimoschema fits none of the scenarios associated with the evolution of high rather than low virulence (e.g. Ewald 1994;Levin and Bull 1994;Nowak and May 1994;Mosquera and Adler 1998;Messenger et al 1999;Vigneux et al 2008;Alizon et al 2009).…”

Section: Discussionmentioning

confidence: 94%

“…Núñez-Farfán et al 2007;Hakes and Cronin 2011). Furthermore, when ancestral and novel hosts are closely related, we would expect similar costs of tolerance in the two hosts and thus selection in the novel host for increasing tolerance (since we expect plants to be relatively intolerant of unfamiliar attackers).…”

Section: Introductionmentioning

confidence: 94%

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Impact of attack by Gnorimoschema gallmakers on their ancestral and novel Solidago hosts

Heard

Kitts

2011

Evol Ecol

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Interactions between insect herbivores and host plants can involve herbivorehost pairs that are evolutionarily ancient or only recently associated. Novel herbivore-host species pairs are continually being formed via host shifts, dispersal, and increasingly via anthropogenic introductions. Conceptual models of enemy-victim coevolution (specifically, the evolution of plant tolerance and of insect virulence) suggest that the impact of an herbivore on its novel host should, at least at first, be more intense than its impact on its ancestral host. We tested this hypothesis for the specialist gallmaking caterpillar Gnorimoschema gallaesolidaginis (Lepidoptera: Gelechiidae) on its ancestral and novel hosts, Solidago altissima and S. gigantea. We measured aboveground ramet mass for paired attacked and unattacked ramets of each species at two sites (Fredericton, NB, and Toronto, ON, Canada), and also measured allocation of tissue mass to stems, leaves, and flowers in galled and ungalled ramets. G. gallaesolidaginis attack reduced ramet growth considerably more on S. gigantea, the novel host, consistent with the coevolutionary hypothesis. We were unable to detect reallocation of tissues in galled ramets as a mechanism for tolerance, and found no intraspecific difference in the impact of gallmaking on allocation patterns. Herbivore host shifts between alternative native hosts will provide an excellent opportunity to understand the evolutionary history of novel herbivore-host associations, particularly (as in the Solidago system) when multiple insect herbivores have host-shifted across the same plant pair.

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