An exotic herbivorous insect drives the evolution of resistance in the exotic perennial herb <i>Solidago altissima</i>

Sakata, Yuzu; Yamasaki, Michimasa; Isagi, Yuji; Ohgushi, Takayuki

doi:10.1890/13-1455.1

Cited by 36 publications

(57 citation statements)

References 63 publications

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“…Consistent with our prediction, infested populations showed higher resistance to the specialist O. communa and lower resistance to the generalists H. armigera and S. litura . While several studies have shown increased resistance to introduced specialist herbivores after re‐exposure to them (Fukano & Yahara, ; Sakata et al, ), our experiment provides the first evidence that such a reassociation can cause a decline in resistance to generalist herbivores. The observed results support the SDH from a new viewpoint.…”

Section: Discussionmentioning

confidence: 47%

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

Wan

Huang

et al. 2018

Journal of Ecology

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The shifting defence hypothesis (SDH) predicts that after invasive plants are introduced to new ranges, they will evolve reduced resistance to specialist herbivores and increased resistance to generalist herbivores because they can escape from specialists but are still attacked by generalists in their nonnative ranges. For this to be true, the subsequent introduction of native specialist herbivores should reverse the above evolutionary processes, but evidence collected so far is scarce. Here, we address this research gap by comparing resistance to specialist and generalist herbivores and resistance‐related traits in the invasive plant Ambrosia artemisiifolia from five populations with about a decade history of infestation by the accidentally introduced native specialist leaf beetle Ophraella communa (infested populations), and three populations without such infestation history (uninfested populations). In common garden experiments, the specialist O. communa performed better on uninfested populations than on infested populations, whereas two generalist insects, Spodoptera litura and Helicoverpa armigera, performed better on infested populations. Chemical analyses showed that plants from infested populations had lower concentrations of chlorogenic acid, an antigeneralist secondary compound that can attract O. communa. Furthermore, across mother plants from all populations studied, chlorogenic acid content was negatively correlated with larval growth of S. litura and positively correlated with that of O. communa. Finally, quantitative defence traits did not differ between infested and uninfested populations. Although our results are most consistent with rapid evolution caused by enemy reassociation, we cannot exclude the possibility that observed differences in resistance result from multiple introductions or selections from other environmental factors. Synthesis. These results suggest that reassociation with a specialist herbivore from the native range may result in a rapid evolution of increased resistance to specialist herbivores and reduced resistance to generalist herbivores in the introduced range, which is likely to be mediated by the reduced production of secondary chemicals that can deter generalists while attracting the introduced specialist. This study supports the shifting defence hypothesis (SDH) from a new viewpoint, emphasizing the importance of incorporating the impacts of both specialist and generalist herbivores when evaluating the long‐term control effects of classical biological control programmes.

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Section: Discussionmentioning

confidence: 47%

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

Wan

Huang

et al. 2018

Journal of Ecology

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“…We measured lace bug population growth and damage level in the fourth week as indices of resistance of S. altissima because the fourth week is an appropriate time for measuring the population growth of lace bugs (Sakata et al. ). Both indices were used to complementarily evaluate plant resistance.…”

Section: Methodsmentioning

confidence: 99%

“…For an index of sexual reproduction, the number of flowers was calculated by the following equation obtained from Sakata et al. (): number of flowers = e 0.11 H + 0.05 W + 3.15 , where H and W are height and width of the capitulescence, respectively. All plants were harvested on 30 November 2013, and the total number of rhizomes was counted and their length was measured.…”

Section: Methodsmentioning

confidence: 99%

“…A previous study demonstrated that this invasion of lace bugs caused rapid evolution of elevated resistance in S. altissima in Japan (Sakata et al. ).…”

Section: Introductionmentioning

confidence: 99%

“…Because lace bugs exert strong selection on resistance in S. altissima in Japan (Sakata et al. ), elucidating the abiotic and biotic factors that determine lace bug density will lead to further understanding of the underlying mechanisms responsible for the evolution of S. altissima resistance during the invasion process. To examine which biotic and abiotic factors drive variation in the density of lace bugs, we conducted the following surveys and experiments.…”

Section: Introductionmentioning

confidence: 99%

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Parallel environmental factors drive variation in insect density and plant resistance in the native and invaded ranges

Sakata

Craig

Itami

et al. 2017

Ecology

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Geographic variation in the traits of a species is shaped by variation in abiotic conditions, biotic interactions, and evolutionary history of its interactions with other species. We studied the geographic variation in the density of the lace bug, Corythucha marmorata, and the resistance of tall goldenrod Solidago altissima to the lace bug herbivory in their native range in the United States and invaded range in Japan. We conducted field surveys and reciprocal transplant experiments to examine what abiotic and biotic factors influence variation in lace bug density, and what ecological and evolutionary factors predict the resistance of the host plant between and within the native and invaded ranges. Lace bug density was higher throughout the invaded range than in the native range, higher in populations with warmer climates, and negatively affected by foliage damage by other insects in both ranges. The higher lace bug density in warmer climates was explained by the shorter developmental time of the lace bugs at higher temperatures. The resistance of S. altissima to lace bugs was higher in populations with lace bugs compared to populations without lace bugs in both native and invaded ranges, indicating that the evolutionary history of the interaction with the lace bugs was responsible for the variation in S. altissima resistance in both ranges. The present study revealed that abiotic and biotic factors, including temperature and other herbivorous insects, can drive the geographic variation in lace bug density, which in turn selects for variation in plant resistance in both in the native and invaded ranges. We conclude that the novel combination of factors such as higher temperature and lower number of other herbivorous insects is responsible for the higher lace bug density in the invaded range than in the native range.

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Different effects of two exotic herbivores on the pollinator‐mediated effect of an exotic plant on a native plant

Sakata

Ueyama

2022

Population Ecology

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Exotic plants can affect native plants indirectly through various biotic interactions. However, combinations of the multiple indirect effects of exotic plants on native plants have been rarely evaluated. Herbivory can either positively or negatively influence plant–pollinator interactions. Here, we addressed whether the pollinator‐mediated plant interaction between exotic and native plants is altered through the introduction of exotic herbivores by conducting a 2‐year common garden experiment. We compared the effects of pollinator‐mediated indirect effects of an exotic plant, Solidago altissima, on the co‐flowering native plant Aster microcephalus in geographically different populations reflecting differences in insect herbivore communities. We found a positive effect of co‐flowering S. altissima on pollinator visitation of A. microcephalus, which varied between gardens and years. The co‐flowering S. altissima did not significantly affect the seed set of A. microcephalus in the first year but had a negative effect in the second year. The facilitative effect of S. altissima on A. microcephalus pollination was suggested to be negatively affected by an exotic aphid, while it was not significantly affected by an exotic lace bug. Our study suggests that the phenology and feeding guilds of the herbivores may be critical for predicting the effect of exotic plants on native plants through herbivore–pollinator interactions. Integrated effects between plant interactions via multiple species interactions under different abiotic and biotic environments are necessary to understand the impact of exotic plants under complex interactions in nature.

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An exotic herbivorous insect drives the evolution of resistance in the exotic perennial herb Solidago altissima

Cited by 36 publications

References 63 publications

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

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

Parallel environmental factors drive variation in insect density and plant resistance in the native and invaded ranges

Different effects of two exotic herbivores on the pollinator‐mediated effect of an exotic plant on a native plant

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