Adaptive impact of the chimeric gene Quetzalcoatl in Drosophila melanogaster

Abstract

Chimeric genes, which form through the genomic fusion of two protein-coding genes, are a significant source of evolutionary novelty in Drosophila melanogaster. However, the propensity of chimeric genes to produce adaptive phenotypic changes is not fully understood. Here, we describe the chimeric gene Quetzalcoatl (Qtzl; CG31864), which formed in the recent past and swept to fixation in D. melanogaster. Qtzl arose through a duplication on chromosome 2L that united a portion of the mitochondrially targeted peptide CG12264 with a segment of the polycomb gene escl. The 3' segment of the gene, which is derived from escl, is inherited out of frame, producing a unique peptide sequence. Nucleotide diversity is drastically reduced and site frequency spectra are significantly skewed surrounding the duplicated region, a finding consistent with a selective sweep on the duplicate region containing Qtzl. Qtzl has an expression profile that largely resembles that of escl, with expression in early pupae, adult females, and male testes. However, expression patterns appear to have been decoupled from both parental genes during later embryonic development and in head tissues of adult males, indicating that Qtzl has developed a distinct regulatory profile through the rearrangement of different 5' and 3' regulatory domains. Furthermore, misexpression of Qtzl suppresses defects in the formation of the neuromuscular junction in larvae, demonstrating that Qtzl can produce phenotypic effects in cells. Together, these results show that chimeric genes can produce structural and regulatory changes in a single mutational step and may be a major factor in adaptive evolution.

Fig. 1.

Structure of a segment of chromosome 2L before (A) and after (B) the formation of Qtzl. Qtzl was formed when approximately 4 kb of sequence encompassing portions of escl and CG12264 experienced a tandem duplication, such that the duplicated 5′ end of CG12264 was united with the duplicated 3′ end of escl. In the diagram, gray areas correspond to 5′ and 3′ UTRs and black lines represent introns. Genes are shaded in blue and yellow to show relationships to parental genes. Full transcript structure and coding sequence boundaries are not depicted for the two pairs of duplicate genes in the region, Ada1-1/Ada1-2 and CG18789/CG18787. The chimeric gene inherits a mitochondrial target peptide (shown in red) from CG12264, a gene that encodes a mitochondrial peptide involved in iron modification of proteins and tRNAs. The 3′ end of Qtzl is inherited out of frame. If translated, the mRNA from Qtzl could encode a peptide of 123 aa.

Fig. 2.

(A) Diversity π, measured as substitutions per site, and (B) Tajima’s D. Both plots are for sliding windows of 10 kb across chromosome 2L. The position of the chimeric gene Qtzl is shown by the open circle and dashed line. Density plots of each metric are juxtaposed to the right of each graph. Both π and D are significantly reduced in the 10-kb window surrounding Qtzl.

Fig. 3.

Local diversity π, measured as substitutions per site, surrounding Qtzl (solid line) fitted with the expectation after a selective sweep (dashed line). The fitted curve describes a selective sweep with s of 0.0098, which occurred 15,000 y ago.