Genetic Variation in Drosophila melanogaster Resistance to Infection: A Comparison Across Bacteria

Abstract

Insects use a generalized immune response to combat bacterial infection. We have previously noted that natural populations of D. melanogaster harbor substantial genetic variation for antibacterial immunocompetence and that much of this variation can be mapped to genes that are known to play direct roles in immunity. It was not known, however, whether the phenotypic effects of variation in these genes are general across the range of potentially infectious bacteria. To address this question, we have reinfected the same set of D. melanogaster lines with Serratia marcescens, the bacterium used in the previous study, and with three additional bacteria that were isolated from the hemolymph of wild-caught D. melanogaster. Two of the new bacteria, Enterococcus faecalis and Lactococcus lactis, are gram positive. The third, Providencia burhodogranaria, is gram negative like S. marcescens. Drosophila genotypes vary highly significantly in bacterial load sustained after infection with each of the four bacteria, but mean loads are largely uncorrelated across bacteria. We have tested statistical associations between immunity phenotypes and nucleotide polymorphism in 21 candidate immunity genes. We find that molecular variation in some genes, such as Tehao, contributes to phenotypic variation in the suppression of only a subset of the pathogens. Variation in SR-CII and 18-wheeler, however, has effects that are more general. Although markers in SR-CII and 18-wheeler explain .20% of the phenotypic variation in resistance to L. lactis and E. faecalis, respectively, most of the molecular polymorphisms tested explain ,10% of the total variance in bacterial load sustained after infection.

The genetic architecture of resistance to virus infection in Drosophila

“…Resistance to bacteria is possibly more polygenic (Lazzaro et al . 2004, 2006), although this may be because true co‐evolved bacterial pathogens of flies have not been isolated. Overall, data from Drosophila support the suggestion that the genetic architecture of susceptibility to infectious diseases may often be simpler than the genetic architecture of susceptibility to noncommunicable diseases (Pritchard 2001; Hill 2012).…”

Genetic architecture of quantitative traits in mice, flies, and humans

“…In mice, quantitative analyses indicate that genotype by environment interaction (GEI) effects occur for all phenotypes, and often makes as large, or larger, contribution to the phenotypic variation than the environmental effects (Valdar et al 2006b). In flies, whenever QTLs have been mapped in different environments, GEI has been observed: for numbers of sensory bristles (Gurganus et al 1998(Gurganus et al , 1999Dilda and Mackay 2002;Geiger-Thornsberry and Mackay 2002), longevity Mackay 2000, 2002;Vieira et al 2000), competitive fitness , and immune response to different bacteria (Lazzaro et al 2006). GEI is mostly attributable to environment-specific expression of QTL alleles, with few cases of opposite effects in different environments .…”

Toll-like receptors — taking an evolutionary approach

“…Thus, Drosophila Toll-like proteins are known to have a range of important roles in development, whereas their role in the control of immune responses is currently limited to Toll. Two other Drosophila TLRs, Toll5 (also known as Tehao) and Toll9, have been linked to an immune function [61][62][63][64] but additional in vivo experiments are needed to clarify this. .…”