Because leaf hairs serve as resistance against herbivores, among‐population variation in hair production may arise from adaptation to local herbivore communities. It is possible that Japanese nettle (Urtica thunbergiana) shows among‐population variation in stinging hair abundance that is associated with the frequency of habitat use by sika deer (Cervus nippon). We examined 31–32 individuals of each of 19 populations for leaf area, stinging hair number (/leaf) and stinging hair density (per square centimeter) in and away from Nara Park (6.6 km2), where many deer have been protected for 1,200 years. At each site we also measured deer habitat use frequency, light intensity and soil fertility as environmental factors potentially affecting leaf traits. We analyzed our hierarchical data at the levels of individuals and populations using multilevel structural equation modeling. Leaf area had a positive direct effect on stinging hair number at the individual level but no significant effect at the population level. At the population level, deer habitat use frequency had a negative direct effect on leaf area and positive direct effects on stinging hair number and density, generating a negative indirect correlation between leaf area and stinging hair number. Light intensity had a negative direct effect on leaf area, while soil fertility had no significant effect on any trait. These results suggest that the relationships between leaf area and stinging hair number at the two levels do not align. We discussed what processes were involved in the effects of environmental factors on leaf traits.
Thorns and hairs of plants can serve as defenses against herbivores, although they may not have evolved under selection by herbivory. Japanese nettles, Urtica thunbergiana, in Nara Park, Nara Prefecture, Japan, where sika deer have been protected for 1200 years, bear many more stinging hairs than those in areas with few or no deer. Previous studies suggested that such hairy nettles evolved under natural selection imposed by intense deer browsing, because stinging hairs deterred deer browsing and because among‐population variation in hair density was associated with deer abundance. To confirm this hypothesis, we examined (1) whether stinging hairs affected oviposition and feeding preferences of herbivorous insects and (2) the degree to which they deterred deer via laboratory and field experiments with hairy nettles from Nara Park and with almost‐hairless nettles from another area. A specialist butterfly, Indian red admiral, showed no oviposition or larval feeding preferences for either hairy or hairless nettles. Insect damage levels did not significantly differ between the two variants. In contrast, deer browsed hairless nettles more heavily than hairy ones. In hairy nettles, however, the level of deer browsing was not proportional to stinging‐hair density, presumably because the hairy nettle population had reached a plateau for resistance as a result of long‐term strong directional selection for stinging hairs. These results corroborate the hypothesis that hairy nettles in Nara Park evolved through natural selection under intense deer browsing.
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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