Experimental test of plant defence evolution in four species using long‐term rabbit exclosures

Didiano, Teresa J.; Turley, Nash E.; Everwand, Georg; Schaefer, Hanno; Crawley, Michael J.; Johnson, Marc T. J.

doi:10.1111/1365-2745.12227

Cited by 33 publications

(42 citation statements)

References 98 publications

(173 reference statements)

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“…, Didiano et al. ). Here, we study the effect of seed predation by Darwin's finches on plant ecology, and its potential role in the evolution of seed defense traits by natural selection.…”

Section: Introductionmentioning

confidence: 99%

The ecology and evolution of seed predation by Darwin's finches on Tribulus cistoides on the Galápagos Islands

Carvajal‐Endara

Hendry

Emery

et al. 2019

Ecological Monographs

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Predator-prey interactions play a key role in the evolution of species traits through antagonistic coevolutionary arms races. The evolution of beak morphology in the Darwin's finches in response to competition for seed resources is a classic example of evolution by natural selection. The seeds of Tribulus cistoides are an important food source for the largest ground finch species (Geospiza fortis, G. magnirostris, and G. conirostris) in dry months, and the hard spiny morphology of the fruits is a potent agent of selection that drives contemporary evolutionary change in finch beak morphology. Although the effects of these interactions on finches are well known, how seed predation affects the ecology and evolution of the plants is poorly understood. Here we examine whether seed predation by Darwin's finches affects the ecology and evolution of T. cistoides. We ask whether the intensity of seed predation and the strength of natural selection by finches on fruit defense traits vary among populations, islands, years, or with varying finch community composition (i.e., the presence/absence of the largest beaked species, which feed on T. cistoides most easily). We then further test whether T. cistoides fruit defenses have diverged among islands in response to spatial variation in finch communities. We addressed these questions by examining seed predation by finches in 30 populations of T. cistoides over 3 yr. Our study reveals three key results. First, Darwin's finches strongly influence T. cistoides seed survival, whereby seed predation varies with differences in finch community composition among islands and in response to interannual fluctuations in precipitation. Second, finches impose phenotypic selection on T. cistoides fruit morphology, whereby smaller and harder fruits with longer or more spines exhibited higher seed survival. Variation in finch community composition and precipitation also explains variation in phenotypic selection on fruit defense traits. Third, variation in the number of spines on fruits among islands is consistent with divergent phenotypic selection imposed by variation in finch community composition among islands. These results suggest that Darwin's finches and T. cistoides are experiencing an ongoing coevolutionary arms race, and that the strength of this coevolution varies in space and time.

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“…, Didiano et al. ). Here, we study the effect of seed predation by Darwin's finches on plant ecology, and its potential role in the evolution of seed defense traits by natural selection.…”

Section: Introductionmentioning

confidence: 99%

The ecology and evolution of seed predation by Darwin's finches on Tribulus cistoides on the Galápagos Islands

Carvajal‐Endara

Hendry

Emery

et al. 2019

Ecological Monographs

Self Cite

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“…Genetic variation in both resistance and tolerance traits has been documented among populations of many plant species (e.g., Fornoni et al 2004;Løe et al 2007;Muola et al 2010a), and such variation has been linked in some species to differences in the intensity of selection exerted by herbivores (Fornoni 2011;Benkman et al 2013;Ågren et al 2013;Didiano et al 2014;Lehndal and Ågren 2015b). However, the extent to which variation in defence against herbivory is correlated with herbivore-mediated selection is poorly known, as is the spatial scale at which such relationships can be detected.…”

Section: Introductionmentioning

confidence: 99%

Herbivory strongly influences among-population variation in reproductive output of Lythrum salicaria in its native range

et al. 2015

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Herbivory can negatively affect several components of plant reproduction. Yet, because of a lack of experimental studies involving multiple populations, the extent to which differences in herbivory contribute to among-population variation in plant reproductive success is poorly known. We experimentally determined the effects of insect herbivory on reproductive output in nine natural populations of the perennial herb Lythrum salicaria along a disturbance gradient in an archipelago in northern Sweden, and we quantified among-population differentiation in resistance to herbivory in a common-garden experiment in the same area. The intensity of leaf herbivory varied >500-fold and mean female reproductive success >400-fold among the study populations. The intensity of herbivory was lowest in populations subject to strong disturbance from ice and wave action. Experimental removal of insect herbivores showed that the effect of herbivory on female reproductive success was correlated with the intensity of herbivory and that differences in insect herbivory could explain much of the among-population variation in the proportion of plants flowering and seed production. Population differentiation in resistance to herbivory was limited. The results demonstrate that the intensity of herbivory is a major determinant of flowering and seed output in L. salicaria, but that differences in herbivory are not associated with differences in plant resistance at the spatial scale examined. They further suggest that the physical disturbance regime may strongly influence the performance and abundance of perennial herbs and patterns of selection not only because of its effect on interspecific competition, but also because of effects on interactions with specialized herbivores.

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“…There are also several studies suggesting that heavy browsing by large mammals causes the v www.esajournals.org KOHyAMA ET AL. evolution of particular defense traits in plants (Stinchcombe and Rausher 2001, 2002, Vourc'h et al 2001, Didiano et al 2014, Martin et al 2015. For example, Martin et al (2015) experimentally documented that populations of orange jewelweed (Impatients capensis) exposed to heavy browsing by white-tailed deer for a long time produce more fruits than those historically protected from deer when plants suffered deer browsing, suggesting that deer browsing imposed selection on tolerance traits in orange jewelweed.…”

Section: Discussionmentioning

confidence: 99%

Differential butterfly performance on host plant variants from populations under intense vs. low mammalian herbivory

et al. 2017

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Abstract. Evolutionary interactions between a pair of species can be modified by the presence of another species that interacts with either or both species. However, only a few studies have demonstrated such complex interactions. Here, we report a case where a population of the red admiral butterfly (Vanessa indica) is assumed to change fitness traits in response to an evolutionary change in its major host plant, the Japanese stinging nettle (Urtica thunbergiana), caused by intense browsing pressure from sika deer (Cervus nippon). Nara Park (NP) in Japan has been home to several hundred protected sika deer for approximately 1200 yr, and their intense browsing pressure is assumed to have selected for heavily haired nettles that are more resistant to deer browsing compared to normal lightly haired nettles occurring in areas with low densities of sika deer. We found that the water and nitrogen contents of leaves are lower and the specific leaf mass is higher in heavily haired nettles at NP compared to the lightly haired nettles at the Takatori Castle Site (TCS) 30 km south of NP. Feeding experiments showed that V. indica larvae from NP reared on heavily haired nettles reach a greater adult body mass and relative abdomen mass than those from TCS, suggesting the possibility that the NP V. indica population has adapted to the heavily haired, nutritionally poorer variant. Analysis of the nucleotide sequence of the mitochondrial cytochrome c oxidase subunit I gene of V. indica from NP and nearby locations including TCS found one haplotype exclusive to NP, suggesting that movement of this butterfly is somewhat restricted. However, analysis using amplified fragment length polymorphism markers showed no genetic differentiation between the seven V. indica populations including the NP and TCS populations. These results suggest that adaptation of the NP population to the heavily haired nettle occurred in a relatively short period. Our study demonstrates a rare example of an indirect evolutionary impact of one herbivore (sika deer) on another herbivore (red admiral butterfly) through an evolutionary change in their shared food plant (Japanese nettle).

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Experimental test of plant defence evolution in four species using long‐term rabbit exclosures

Cited by 33 publications

References 98 publications

The ecology and evolution of seed predation by Darwin's finches on Tribulus cistoides on the Galápagos Islands

The ecology and evolution of seed predation by Darwin's finches on Tribulus cistoides on the Galápagos Islands

Herbivory strongly influences among-population variation in reproductive output of Lythrum salicaria in its native range

Differential butterfly performance on host plant variants from populations under intense vs. low mammalian herbivory

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