A facultative ectoparasite attains higher reproductive success as a parasite than its free-living conspecifics.

Comparative and phylogenetic studies reveal that parasites evolved from free-living ancestors, but the underlying processes and mechanisms are not well understood. In order for selection to favor the evolution of parasitism, there must be pre-existing adaptations for host exploitation and a fitness advantage favoring the transition to parasitism. Here, we experimentally investigate the differential reproductive success of a facultative parasite, Macrocheles subbadius. Lifetime reproductive success was higher among female mites that fed on fruit fly hemolymph as parasites compared to free-living mites. The per capita lifetime fecundity for parasitic females was 2.4 times that of free-living females. The offspring sex ratio also differed between the two modes of life, with parasitic mites producing more sons and hence a relatively weaker female-biased sex ratio (0.61) than mites that were free-living (0.94). These results suggest that parasitic female mites allocate more resources to egg production, and were limited by sperm rather than food, as was the case with free-living mites. The higher lifetime reproductive success of mites that opportunistically feed on host hemolymph provides the fitness advantage necessary for the evolution of parasitism.