Yellow shapes mosquito pigmentation and vector competence to Plasmodium berghei

Abstract

The insect-specific yellow gene, first described over a century ago, remains enigmatic despite its conserved role in pigmentation. In the malaria vector mosquito Anopheles coluzzii, yellow is strongly expressed during juvenile stages and in adult ovaries, mirroring pigmentation patterns that likely enhance desiccation resistance, camouflage, and reproductive fitness. To dissect its function, we generated a complete knockout allele yellow(-)KI by replacing the first exon with an EGFP reporter, and introgressed it into multiple genetic backgrounds. Loss of yellow abolished black cuticle pigmentation and delayed larval development but left adult lifespan unaffected. Developmental delay likely impaired mating success in competition with wild-type mosquitoes, hastening the decline of the X-linked yellow(-)KI allele. Notably, yellow(-)KI females showed a consistent twofold increase in susceptibility to the rodent malaria parasite Plasmodium berghei, independent of the complement factor TEP1 and melanization, whereas infection with P. falciparum was unchanged. Antibiotic treatment reversed the heightened P. berghei susceptibility, implicating altered gut microbiota as a mediator. Our findings reveal that yellow not only shapes pigmentation but also indirectly modulates vector competence through microbiota-dependent mechanisms, underscoring the complex interplay between cuticle biochemistry, microbial ecology, and pathogen transmission.