Population genetics of the developmental gene optomotor-blind (omb) in Drosophila polymorpha: evidence for a role in abdominal pigmentation variation

Abstract

The developmental gene optomotor-blind (omb) encodes a T-box-containing transcription factor that has multiple roles in Drosophila development. Previous genetic analyses established that omb plays a key role in establishing the abdominal pigmentation pattern of Drosophila melanogaster. In this report we examine patterns of omb nucleotide variation in D. polymorpha, a species that is highly polymorphic for the phenotype of abdominal pigmentation. Haplotypes at this locus fall into two classes that are separated by six mutational steps; five of these mutational events result in amino acid changes. Two lines of evidence are consistent with a role for omb in the abdominal pigmentation polymorphism of D. polymorpha. First, we find that haplotype classes of omb are correlated with abdominal pigmentation phenotypes, as are microsatellite repeat numbers in the region. Second, tests of selection reveal that the two haplotype classes have been maintained by balancing selection. Within each class there is a significantly low amount of diversity, indicative of previous selective sweeps. An analysis including D. polymorpha's closest relatives (members of the cardini group) provides evidence for directional selection across species. Selection at this locus is expected if omb contributes to variation in abdominal pigmentation, since this trait is likely of ecological importance.

Figure 1.—

(A) The omb locus of D. melanogaster showing the distribution of exons (numbered) in boxes and introns as lines. (B) Areas of omb used in this study, including portions of the N-terminal domain and the T-domain. Arrows represent locations of primers used for PCR amplification.

Figure 2.—

Alignment of N-terminal region omb haplotypes from five divergent species of Drosophila. Letters are the common amino acid designations, and periods represent gaps introduced for alignment.

Figure 3.—

(A) Tree constructed from omb N-terminal haplotypes culled of microsatellite repeats and (B) tree constructed from omb N-terminal haplotypes including information from two microsatellite repeats. Each circle represents a single haplotype, the circle is sized relative to the number of individuals of each observed haplotype, each line is a single mutational step, and empty circles are unobserved haplotypes.

Figure 4.—

Alignment of five representative D. polymorpha omb N-terminal amino acid sequences. Underlined areas are variable microsatellite regions and asterisks mark polymorphic amino acid sites.

Figure 5.—

Linkage disequilibrium between microsatellite runs in the N-terminal region of omb in D. polymorpha. “AA” refers to the amino acids that characterize the distinction between allele classes A and B. The association between pairs marked with two asterisks is P < 0.01, those with one asterisk are 0.01 < P < 0.05, and “ns” indicates no association.

Figure 6.—

Nesting design used for the nested clade analyses for the haplotype tree created from the omb N-terminal sequences (A) culled of microsatellites and (B) with information from two microsatellites. Solid lines outline one-step clades. Broken lines outline two-step clades. The heavy dark line separates three-step clades.