Generalist insect herbivores, such as the phloem-feeding whitefly Bemisia tabaci, can rapidly adapt to a broad range of suitable host plants. However, their adaptation mechanisms, when restricted to novel and marginally suitable hosts over multiple generations, remain poorly understood. We established a multi-generational experimental system using B. tabaci populations reared for over 34 generations on either cotton (suitable host) or habanero-pepper (marginally-suitable host with initial survival of <5%) to investigate performance, gene expression, and genomic regulation.
Reciprocal host performance tests at optimal (30 °C) and mild-stress (24 °C) conditions revealed that the pepper-adapted population increased survival on habanero pepper to >60%, albeit with reduced fitness on cotton and sensitivity to temperature stress. Transcriptomic analysis showed significant upregulation of cuticle structural genes and downregulation of cysteine-type peptidases, including cathepsin B, which may attenuate plant defense activation.
We further examined the roles in adaptation to habanero-pepper of changes in epigenetic patterning (alterations in DNA methylation) and sequence variation in promoter regions. While overall DNA methylation patterns differed between host-adapted populations, methylation changes did not correlate directly with expression levels. Instead, a functional pattern emerged: housekeeping genes were hypermethylated with stable expression, while environmental-response genes were hypomethylated and highly variable. Promoter variation analyses suggested selection for alleles potentially contributing to host adaptation.
Our findings suggest that both epigenetic mechanisms and genetic variation contribute to adaptive responses in generalist herbivores, facilitating survival and performance on novel, suboptimal hosts across generations.
