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Evolutionary transition from blood feeding to obligate nonbiting in a mosquito

W. Bradshaw,Joshua G. Burkhart,J. Colbourne,Rudyard J. Borowczak,Jacqueline Lopez,D. Denlinger,Julie A. Reynolds,M. Pfrender,C. Holzapfel

Published 2017 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance The evolutionary transformation from a blood-feeding to an obligate nonbiting lifestyle is occurring uniquely within the genetic background of a single species of mosquito, Wyeomyia smithii, as a product of selection in nature. Associated genetic changes in metabolic pathways indicate a high anticipatory metabolic investment prior to consuming blood, presumably balanced by the reproductive benefits from an imminent blood meal. This evolutionary transformation provides a starting point for determining pivotal upstream genetic changes between biters and nonbiters and for identifying universal nonbiting genes or pathways in mosquitoes. If there is no bite, there is no transmission of pathogens; hence W. smithii offers a different approach to investigate control of blood-feeding vectors of human diseases. The spread of blood-borne pathogens by mosquitoes relies on their taking a blood meal; if there is no bite, there is no disease transmission. Although many species of mosquitoes never take a blood meal, identifying genes that distinguish blood feeding from obligate nonbiting is hampered by the fact that these different lifestyles occur in separate, genetically incompatible species. There is, however, one unique extant species with populations that share a common genetic background but blood feed in one region and are obligate nonbiters in the rest of their range: Wyeomyia smithii. Contemporary blood-feeding and obligate nonbiting populations represent end points of divergence between fully interfertile southern and northern populations. This divergence has undoubtedly resulted in genetic changes that are unrelated to blood feeding, and the challenge is to winnow out the unrelated genetic factors to identify those related specifically to the evolutionary transition from blood feeding to obligate nonbiting. Herein, we determine differential gene expression resulting from directional selection on blood feeding within a polymorphic population to isolate genetic differences between blood feeding and obligate nonbiting. We show that the evolution of nonbiting has resulted in a greatly reduced metabolic investment compared with biting populations, a greater reliance on opportunistic metabolic pathways, and greater reliance on visual rather than olfactory sensory input. W. smithii provides a unique starting point to determine if there are universal nonbiting genes in mosquitoes that could be manipulated as a means to control vector-borne disease.

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