Integrative analysis of fine-scale local adaptation of winter moths to variable oak phenology

Abstract

For herbivorous insects whose fitness depends on tight phenological synchrony with host plants, spatial variation in plant phenology can impose strong selective pressures and promote local adaptation to host timing. These dynamics are central to predicting how species will respond to environmental change, particularly climate-driven shifts in plant phenology. The winter moth (Operophtera brumata) relies on synchronising larval egg hatch with leaf budburst of deciduous trees, yet whether they are locally adapted to their hosts phenology, and their capacity to track future change, remains unclear. Here, we investigated potential small-scale local adaptation of winter moths to oak tree phenology in Wytham Woods, UK, a 385-hectare woodland, within which oak budburst can vary by up to three weeks within a given year. We conducted laboratory temperature manipulation experiments using 76 clutches across six temperature treatments, and field translocation experiments using over 200 clutches. We combined these experiments with assessment of population structure from whole-genome sequencing of 59 individuals. This integrative approach allowed us to assess local adaptation in terms of phenotypic differences, fitness consequences, and genetic evidence. Temperature manipulations revealed systematic differences in the timing of egg hatching across temperature treatments at the clutch level which were linked to carry-over effects from the mothers emergence time, but unrelated to their source tree budburst timing. Field translocation experiments further showed no significant differences in survival of individuals transplanted to trees with phenology differing from their original host tree, and there was no genetic structure across the population. Together, these results reveal consistent differences in hatching phenology despite the absence of population structure, strong selection, or accordance with relative tree phenology. Our findings advance our understanding of the mechanisms maintaining close synchrony in trophic interactions at small scales, which may drive spatial variation in evolutionary responses to future climate change.