New genes in Drosophila quickly become essential

Abstract

To investigate the origin and evolution of essential genes, we identified and phenotyped 195 young protein-coding genes, which originated 3 to 35 million years ago in Drosophila. Knocking down expression with RNA interference showed that 30% of newly arisen genes are essential for viability. The proportion of genes that are essential is similar in every evolutionary age group that we examined. Under constitutive silencing of these young essential genes, lethality was high in the pupal stage and also found in the larval stages. Lethality was attributed to diverse cellular and developmental defects, such as organ formation and patterning defects. These data suggest that new genes frequently and rapidly evolve essential functions and participate in development.

Fig. 1.

Origin of new essential genes during recent evolution in Drosophila. (A) Schematic representation for the hypothesis for the origin of a new essential gene. The ancestral species D is immediately before the new gene X originated. (B) Number of young essential genes in major evolutionary periods [D/R and A represent DNA/RNA-based duplicate genes and de novo genes with examples in (C) to (E), respectively]. The subtotal for a particular mechanism, including both essential and nonessential genes, is also shown as a denominator in B. Green, yellow, red and boxes represent exons in the parental genes, young genes, and recruited chimeric regions, respectively. Dashed lines represent paralogous duplicated regions.

Fig. 2.

Staging lethality of gene silencing by fluorescence tracking. Living flies with RNAi–green fluorescent protein dual constructs are shown for six major D. melanogaster developmental stages: L1, first instar larva; L2, second instar larva; L3, third instar larva; EP, early pupa; PH, pharate (late pupa); A, adult. (Right) Genotypes of the flies. (Left) Stage of lethality. N.S., no flies of this genotype survived to this stage.

Fig. 3.

Representative cellular and developmental defects. Representative tissue-specific LOF of young essential genes leading to (A) defects in notum scutellar morphologies, (B) irregular bristle patterning and loss of bristles, (C) necrosis and tissue death at multiple places in the notum, (D) tumor formation at the junction between scutum and scutellum, (E) loss of asymmetric patterning with mirror-like wings and ectopic bristles, and (F) possible signaling defect with wing notches. Genotypes of flies are shown above each image, with scale bars in the lower right corners. Yellow arrowheads point to particular phenotypic defects.