Fine-scale frequency differentiation along a herbivory gradient in the trichome dimorphism of a wild Arabidopsis

Geographic variation is commonly observed in plant resistance traits, where plant species might experience different selection pressure across a heterogeneous landscape. Arabidopsis halleri subsp. gemmifera is dimorphic for trichome production, generating two morphs, trichome-producing (hairy) and trichomeless (glabrous) plants. Trichomes of A. halleri are known to confer resistance against the white butterfly, cabbage sawfly, and brassica leaf beetle, but not against flea beetles. We combined leaf damage, microclimate, and microsatellite loci data of 26 A. halleri populations in central Japan, to explore factors responsible for fine-scale geographic variation in the morph frequency. We found that hairy plants were less damaged than glabrous plants within populations, but the among-site variation was the most significant source of variation in the individual-level damage. Fixation index (G(st)'') of a putative trichome locus exhibited a significant divergence along population-level damage with an exception of an outlier population, inferring the local adaptation to herbivory. Notably, this outlier was a population wherein our previous study reported a balancing role of the brassica leaf beetle Phaedon brassicae on the morph frequency. This differentiation of the trichome locus was unrelated to neutral genetic differentiation (evaluated by G(st)'' of microsatellite loci) and meteorological factors (including temperature and solar radiation). The present findings, combined with those of our previous work, provide suggestive evidence that herbivore-driven divergence and occasional outbreak of a specific herbivore have jointly contributed to the ecogeographic pattern in the frequency of two morphs.