Costs of Resistance in the Drosophila?macrocheles System: A Negative Genetic Correlation Between Ectoparasite Resistance and Reproduction

Abstract

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 • to 29 • 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.

Condition, innate immunity and disease mortality of inbred crows

“…Factors that might potentially predispose inbred individuals to disease include differences in behavioural resistance (Calleri et al 2006;Luong & Polak 2007) or immune response (Reid et al 2007), which might be owing, in part, to differences in condition or nutrition (Moller et al 1998;Blanco et al 2001;Koski & Scott 2001) among individuals with different inbreeding coefficients. Previous field studies have explored links between inbreeding and components of the immune response (Reid et al 2007), inbreeding and disease (e.g.…”

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system

“…Previously, we demonstrated that resistance-selected lines experience a significant reduction in female fecundity, and that this effect is temperature-dependent (Luong and Polak, 2007). In the present study, we test for genetic trade-offs between ectoparasite resistance and larval competitive ability in lines of Drosophila nigrospiracula selected for resistance against an ectoparasitic mite.…”

“…Moreover, heritable genetic variation for this behavioral form of resistance has been documented in natural populations. Heritability for resistance was previously estimated to be 0.12-0.15 (Polak, 2003;Luong and Polak, 2007), demonstrating that additive genetic variation for ectoparasite resistance exists in natural populations.…”

“…By including the latter category, we were able to test for any difference between the base and control lines. This baseline check provides a means of evaluating whether differential inbreeding depression may be playing a role in the expression of any fitness costs, or whether larval competitive ability evolved in the control lines during the course of the experiment, for example, by random genetic drift; either of these factors can confound interpretation of any observed differences between selected and control lines (Luong and Polak, 2007).…”

“…Given the considerable fitness consequences of parasitism, and hence directional selection for increasing resistance, fly populations, all else being equal, are expected to evolve highest values of resistance against ectoparasitism. However, significant genetic heterogeneity for resistance persists in natural populations (Polak, 2003;Luong and Polak, 2007).…”