A Selective Sweep Likely Linked to Xenobiotic Detoxification Identified Along Altitudinal Gradients in the Pine Processionary Moth.

Abstract

Understanding how natural populations adapt to complex environmental gradients is crucial for predicting evolutionary responses to global change. The pine processionary moth (Thaumetopoea pityocampa), a major forest pest expanding northward and upward in Europe, provides an ideal model to explore genomic adaptation along altitudinal and/or latitudinal gradients. We combined pooled and individual whole-genome resequencing of four pairs of low- and high-elevation populations from Spain, Italy, and France (mainland and Corsica) to detect signatures of local adaptation. Population structure analyses revealed strong differentiation among distant populations but limited divergence within altitude pairs. Genome scans identified a few candidate regions under selection, and we notably uncovered a large (∼1 Mbp) region showing reduced nucleotide diversity, negative Tajima's D, and fixed allele differences between high- and low-altitude populations, consistent with a recent selective sweep. This region includes a cluster of cytochrome P450 genes and the voltage-gated sodium channel gene para, both involved in detoxification and insecticide resistance. Although signatures of selection were observed at this locus in two distant population pairs, no definitive evidence of recent introgression was found between these distant populations, suggesting independent evolution. Altogether, our results do not show clear evidence for altitudinal adaptation in T. pityocampa but suggest that xenobiotic exposure could exert a strong selective pressure locally. Our study highlights candidate genes and regions for further investigation of resistance evolution in an insect species in the wild.