Costs of resistance in the Drosophila-macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction

Genetic variation for parasite resistance occurs in most host populations. Costs of resistance, manifested as reduced fitness of resistant genotypes in the absence of parasitism, can be an important factor contributing to the maintenance of this variation. One powerful tool for detecting costs of resistance is the study of correlated responses to artificial selection. Provided that experimental lines are recently derived from large outbreeding populations, and that inbreeding is minimized during the experiment, correlated responses to selection are expected to be strong indicators of pleiotropy. We artificially selected for elevated behavioral resistance against an ectoparasitic mite (Macrocheles subbadius) in replicate populations of the fly Drosophila nigrospiracula. Resistance was modeled as a threshold trait, and the realized heritability of resistance was estimated to be 12.3% (1.4% SE) across three replicate lines recently derived from nature. We contrasted the longevity and fecundity of resistant and control (unselected) flies under a variable thermal environment. We report that reduced fecundity is a correlated response to artificial selection for increased resistance, and that the strength of this effect increases from 25 degrees to 29 degrees C. In contrast, longevity differences were not detected between resistant and control lines at either temperature. These findings are robust as they were confirmed with an independent set of experimental lines. Thus, our results identify a negative genetic correlation between ectoparasite resistance and an important life-history trait. That a correlated response was only detected for fecundity, and not longevity, suggests that the genetic correlation is attributable to pleiotropic effects with narrower effects than reallocation of a general resource pool within the organism, although other interpretations are discussed. Combined with fluctuating parasite-mediated selection and temperature, the presence of this trade-off may contribute to the maintenance of genetic variation for resistance in natural populations.