Comparative metabolomics reveal developmental and ecological plasticity in the invasive parasite Philornis downsi (Diptera: Muscidae) from the Galapagos Islands.

Invasive species pose a critical threat to biodiversity, often endangering ecologically naive endemic fauna. The avian vampire fly, Philornis downsi Dodge & Aitken, 1968 (Diptera: Muscidae), a semi-hematophagous ectoparasite introduced to the Galápagos Islands, has caused severe declines in endemic and native bird populations, including Darwin's finches. Yet, the physiological mechanisms enabling its ecological success remain largely unexplored. Here, we describe the first metabolome study of P. downsi, identifying 806 metabolites (78% confirmed by standards) across 2 developmental stages (larvae and adults) and from 2 ecological contexts (collected from natural habitats and reared under laboratory conditions). Global metabolomics analysis revealed pronounced stage- and sex-specific metabolic reprogramming in response to ecological context. Wild females showed enriched pathways linked to reproductive investment and environmental resilience, including α-linolenic acid, nicotinamide, and ascorbate metabolism. Wild males exhibited elevated lipid signaling, one-carbon metabolism, and phosphonate pathways, suggesting adaptations to reproductive demands and environmental variability. In contrast, lab-reared adults displayed more constrained metabolic profiles dominated by carbohydrate and vitamin metabolism, indicative of physiological canalization under nutrient-rich conditions. Larvae exhibited the most extensive metabolic divergence. Wild larvae were enriched in pathways related to amino acid turnover, antioxidant defenses, and membrane lipid remodeling, patterns reflecting developmental plasticity under fluctuating ecological pressures. Lab-reared larvae, conversely, exhibited upregulation in fructose and mannose metabolism, phenylalanine metabolism, and starch and sucrose metabolism, likely reflecting metabolic optimization for growth efficiency. These findings provide molecular insight into the physiological plasticity and invasion success of P. downsi, informing refinements in mass rearing for control strategies.