Evolved Transcriptional Responses and Their Trade-Offs after Long-Term Adaptation of Bemisia tabaci to a Marginally Suitable Host

Abstract

Although generalist insect herbivores can migrate and rapidly adapt to a broad range of host plants, they can face significant difficulties when accidentally migrating to novel and marginally-suitable hosts. What happens, both in performance and gene expression regulation, if these marginally-suitable hosts must be used for multiple generations before migration to a suitable host can take place, largely remains unknown. In this study, we established multigenerational colonies of the whitefly Bemisia tabaci, a generalist phloem-feeding species, adapted to a marginally-suitable host (habanero pepper) or an optimal host (cotton). We used reciprocal host tests to estimate the differences in performance of the populations on both hosts under optimal (30 oC) and mild-stressful (24 oC) temperature conditions, and documented the associated transcriptomic changes. The habanero pepper-adapted population greatly improved its performance on habanero pepper but did not reach its performance level on cotton, the original host. It also showed reduced performance on cotton, relative to the non-adapted population, and an antagonistic effect of the lower-temperature stressor. The transcriptomic data revealed that most of the expression changes, associated with long-term adaptation to habanero pepper, can be categorized as “evolved” with no initial plastic response. Three molecular functions dominated: enhanced formation of cuticle structural constituents, enhanced activity of oxidation-reduction processes involved in neutralization of phytotoxins and reduced production of proteins from the cathepsin B family. Taken together, these findings indicate that generalist insects can adapt to novel host plants by modifying the expression of a relatively small set of specific molecular functions.

An association betweenDnmt1andWntin the production of oocytes in the whiteflyBemisia tabaci

“…However, Dnmt1 expression was reduced, and the magnitude of reduction observed here has been shown to reduce the presence its protein, DNMT1, within the nucleus of ovarian cells (Shelby et al, 2023). The observed amount of differentially expressed genes is reasonable from whole bodies of this species when the experimental effects are regional or tissue specific (Tadmor et al, 2022). A second possible explanation is that we did not detect high levels of differentially expressed genes because we did not appreciably reduce DNA cytosine methylation.…”

“…One possible explanation for detecting few differential expressed genes is that we were not sampling only the tissue in which Dnmt1 knockdown has its effect, the ovaries, but rather sampling whole bodies. However, Dnmt1 expression was measurably reduced, and this treatment is known to reduce the presence of its protein, DNMT1, within the nucleus of ovarian cells of Dnmt1 knockdowns (Shelby et al, 2023) and this magnitude of differences is reasonable from whole bodies of this species when the experimental effects are regional or tissue specific (Tadmor et al, 2022). A second possible explanation is that we did not detect high levels of differentially expressed genes because we did not appreciably reduce DNA cytosine methylation.…”

Adaptation of an arthropod predator to a challenging environment is associated with a loss of a genome‐wide plastic transcriptional response

“…Interestingly, we identified 124 DEGs shared between cucumber‐reared P. persimilis (26% of all DEGs on cucumber) and bean‐reared P. persimilis exposed to tomato for 48 h. The GO term ‘the structural component of cuticle’ was enriched in this gene group. Because this GO term is often enriched in transcriptomic comparisons involving arthropod transfer to a new host plant, 77 it is hypothesized that it may signify a non‐specific response to a new host plant environment. As such, we could also postulate that the large proportion of differential expression, including structural components of the cuticle, may signify continued stress of P. persimilis on cucumber.…”

Whitefly–Plant Interactions: An Integrated Molecular Perspective

“…These gene families are expanded (1.7-to 2.5-fold) in the B. tabaci genome relative to those of other closely related phloemfeeding insects (17,90,165). In addition, these genes display marked changes in their expression when whiteflies shift between host plants (91,111,135,159). The differential expression of GH13 enzyme and sugar transporter genes during host shifts may allow whiteflies to maintain sugar homeostasis (91).…”

“…Their overor underexpression could be related to changes in the whitefly's ability to degrade phloem proteins for nitrogen salvaging and/or to counteract plant defenses (40,117). Lastly, during long-term (multiple generations) adaptation to a well-defended host plant, both B. tabaci and T. vaporariorum overexpress large numbers of genes encoding structural constituents of the insect cuticle (Gene Ontology 0042302) (111,135). The possible role this function plays in whitefly host adaptation remains unclear but may relate to physical changes (e.g., exoskeleton hardening, increased body volume and/or muscle content) that enhance survivorship and reproduction on well-defended plants.…”