Genomic basis of adaptation to constant and fluctuating environments in a global pest of cereals

In agricultural systems, spatially and temporally heterogeneous environments are expected to favour the evolution of generalist pests and pathogens, yet the genomic mechanisms underlying niche-breadth expansion remain poorly understood. Here, we address this gap by assembling one of the smallest known eukaryotic genomes--from the global cereal pest Aceria tosichella--and by resequencing generalist and specialist populations which evolved in the lab on constant versus fluctuating hosts. A previous study demonstrated that generalist populations retained a wider niche, including the ability to exploit a refuge host, compared to specialist populations that showed a narrowing of the ecological niche. Genomic scans identified 640 SNPs that significantly differed in frequency between treatments, including a single highly differentiated 120-kbp region containing 13 genes. Allele-frequency shifts across many SNPs in this region paralleled phenotypic divergence in the ability to utilise refuge hosts, and gene annotations suggested their roles in starvation resistance and nutrient signalling. However, experimental validation of the top candidate gene did not support its strong direct effect on survival on the refuge host, implying a more complex, likely polygenic basis for adaptation. Consistent with this interpretation, numerous significant SNPs occurred outside the focal region, with enrichment for genes involved in xenobiotic transport, detoxification pathways, and ABC transporters. Together, these results indicate that generalism in A. tosichella relies on complex molecular mechanisms that enable survival on suboptimal or refuge hosts, relying to a considerable extent on the ability to deal with stress arising, for example, from toxic compounds present in suboptimal hosts.