Contemporary ecological heterogeneity shapes candidate adaptive genomic variation across the native range of an invasive herbivore

Abstract

Ecological heterogeneity within a species native range can shape genomic variation available for subsequent range expansion and biological invasion. The cactus moth, Cactoblastis cactorum, is a South American oligophagous herbivore on Opuntia that has become an invasive pest outside its native range. In Argentina, populations span wide climatic and geographic gradients and exploit both native Opuntia species and the introduced crop O. ficus-indica. Using ddRADseq data from 136 individuals across 28 populations, we combined genome-wide differentiation scans (XtX), a host-use contrast, and genotype-environment association (GEA) analyses to identify candidate genomic signatures associated with contemporary ecological variation. XtX analyses detected 12 candidate regions, whereas the host-use contrast identified 17 regions differentiating populations sampled from O. ficus-indica and native Opuntia, several of which persisted in a geographically restricted sensitivity analysis. GEA analyses identified 167 covariate-specific loci, including candidate genes associated with detoxification and metabolism (CYP6B2), oxygen-sensing pathways (Egln1), and circadian regulation (TIMELESS). Convergence among analyses was limited but stronger than expected by chance. Temperature-associated loci in fax and Bag6 occurred within an XtX candidate region, whereas Hspg2 was independently recovered in host-use and environmental analyses and retained after geographic restriction. Most candidate variants occurred in non-coding genomic contexts, protein-altering variants were uncommon, and candidate genes spanned diverse functions, consistent with a potentially regulatory and polygenic architecture of adaptation. Overall, our results reveal a heterogeneous genomic landscape associated with climatic variation and introduced-host use, with recurrent loci providing the strongest evidence for localized adaptive differentiation across the native range of C. cactorum.