Linkage disequilibrium and recent selection at three immunity receptor loci in Drosophila simulans

Abstract

Immune system genes in a California population sample of Drosophila simulans were shown to bear several hallmarks of the effects of past directional selection. One potential effect of directional selection is an increase in linkage disequilibrium among the polymorphic sites that are linked to the site under selection. In this study, we focus on three D. simulans immunity loci, Hmu, Sr-CI/Sr-CIII, and Tehao, for which the polymorphic sites are in nearly perfect linkage disequilibrium, an unusual finding even with respect to other immunity genes sampled from the same lines. The most likely explanation for this finding is that, at each locus, two divergent alleles have been selected to intermediate frequencies in the recent past. The extent to which the linkage disequilibrium extends to the flanks of each of the immunity genes is minimal, suggesting that the favored mutations actually occurred within the immunity genes themselves. Furthermore, the excess linkage disequilibrium found in the California population is not found in an African D. simulans population sample and may be a result of novel pathogen-mediated selection pressures encountered during establishment of non-African populations.

Figure 1.—

(a) Linkage disequilibrium (Z_nS) values in D. simulans immunity, nonimmunity autosomal, and nonimmunity X-linked genes from the CA1 population sample. Outlier genes are identified. (b) Nucleotide heterozygosity (θ) in the same genes.

Figure 2.—

Polymorphism tables for Hmu, Sr-CI/Sr-CIII, and Tehao from the CA1 population sample. Position refers to the nucleotide position in the alignment; type refers to noncoding, silent, or replacement mutations; and dashes represent identity to the allele at first sequence.

Figure 3.—

LD values at loci to the flanks of Hmu, Sr-CI/Sr-CIII, and Tehao in the CA1 population sample.