The shared vulnerability network of biothreats: A coupled framework linking feeding biology, plant immunity, vector competence and insecticide resistance in sap-sucking insects under climate change

Abstract

Sap-sucking insect pests, including whiteflies, aphids, thrips, leafhoppers, planthoppers and psyllids, are conventionally investigated as separate biological and management problems, with feeding injury, virus transmission and insecticide resistance typically addressed by different research communities. This review argues that such separation reflects disciplinary organisation rather than the underlying biology of these insects. Using whitefly-centred evidence and extending the synthesis comparatively to other major sap-sucking taxa, we demonstrate that four processes traditionally considered independent-phloem-feeding physiology, plant immune signalling, virus vector competence and insecticide resistance evolution-converge on a limited set of shared physiological currencies, including osmoregulatory and detoxification systems, obligate and facultative endosymbionts and the duration of sustained phloem ingestion. Because these physiological currencies are shared, interventions or environmental changes affecting one process can propagate across the others, generating system-wide consequences. We formalise these interactions as the shared vulnerability network (SVN), a conceptual framework in which feeding biology, plant immunity, vector competence and resistance evolution form four interconnected interfaces collectively modulated by climate change. Using this framework, we synthesise the primary literature on sap-sucking insect diversity, host plant resistance (HPR), virus transmission biology, insecticide resistance evolution, RNA interference and other precision-management technologies while explicitly distinguishing well-established knowledge from emerging, field-unvalidated approaches. Finally, we identify specific, testable research priorities that arise directly from the framework and argue that durable, climate-resilient pest management requires evaluating interventions for their consequences across the entire coupled system rather than their effectiveness against a single life stage, physiological process or biochemical target in isolation.