A systematic review of locust phase polyphenism: from proximate mechanisms to ecology and management.

内容摘要

Locust phase polyphenism is a remarkable example of phenotypic plasticity, driven by population density to produce a dramatic shift between cryptic, solitarious and swarming, gregarious phenotypes. Despite over a century of research, the evidence base lacks systematic synthesis. We conducted a systematic review of 400 studies on locust phase polyphenism, integrating evidence across ecological, neurobiological, physiological, molecular, epigenetic, and microbial drivers. The results revealed that the evidence base is constrained by two critical limitations. First, severe taxonomic narrowness: 93.8% of studies focus on at least one of two model species (desert locust, Schistocerca gregaria and migratory locust, Locusta migratoria), with only 6.2% examining other locust species exclusively. Second, profound methodological disconnect: 84.5% of studies are laboratory-based, while field-only (6.0%) and integrated field-laboratory studies (6.2%) together constitute only 12.2% of the literature. Within this paradigm, mechanistic research has successfully mapped proximate pathways from tactile stimulation and serotonin/dopamine signaling to transcriptomic reprogramming and epigenetic regulation. However, direct species comparisons reveal fundamental divergence rather than conservation, challenging assumptions of universal mechanisms. Laboratory-derived pathways remain poorly integrated with field ecology-vegetation structure, nutritional geography, and climate dynamics-creating a translational impasse for predictive management. Emerging areas such as microbiome dynamics and transgenerational epigenetics require causal validation under ecologically relevant conditions. Reliance on the current narrow paradigm fundamentally limits both biological understanding and practical application. We propose a future research prioritizing: (1) phylogenetically broad comparative multi-omics to distinguish conserved cores from lineage-specific adaptations; (2) integrated field-laboratory experiments incorporating climate and landscape heterogeneity; (3) causal validation of emerging regulators in ecologically relevant contexts; and (4) translation of comparative insights into species-specific management tools through equitable partnerships with researchers and practitioners in outbreak-affected regions. Such integration is essential for developing predictive, sustainable management strategies in an era of global change.