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

Abstract

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).