Origin and spread of de novo genes in Drosophila melanogaster populations

Abstract

Comparative genomic analyses have revealed that genes may arise from ancestrally nongenic sequence. However, the origin and spread of these de novo genes within populations remain obscure. We identified 142 segregating and 106 fixed testis-expressed de novo genes in a population sample of Drosophila melanogaster. These genes appear to derive primarily from ancestral intergenic, unexpressed open reading frames, with natural selection playing a significant role in their spread. These results reveal a heretofore unappreciated dynamism of gene content.

Fig.1

Basic properties of segregating de novo genes. (A). Expression estimates of segregating de novo genes, fixed de novo genes, all annotated genes and annotated male-biased genes in D. melanogaster. (B). Simulation of de novo gene locations. The boxplot for each chromosome is the simulated number of genes from intergenic regions. The black dot is the observed number. The X chromosome is the only chromosome arm that deviates from the expected number of genes (t-test, p=0.01).(C). Pie chart of segregating de novo gene frequency.

Fig. 2

Regulation and population genetics of segregating de novo genes. (A). Potential cis-regulatory elements. The most common shared 8 bp and 10 bp consensus motifs in 5’–flanking regions are listed. From top to bottom, 34, 29, 25 and 30 multiple-exon genes show these motifs. (B). Nucleotide diversity (π for de novo genes and flanking regions. Red line: π expressing lines/π non-expressing lines; green line: expected values from re-sampling of intergenic DNA conditional on same derived allele frequency distribution as observed de novo genes. π estimates for 5’ and 3’ flanking regions of genes were incremented in 5kb windows. (C). A gene (Gene_X_141) that may have experienced a hard selective sweep. Grey box: expressed lines. The TSS region contains a derived allele fixed in expressing strains and absent in non-expressing strains; flanking regions are homozygous in expressing strains. (D). A gene (Gene_3L_079) showing no evidence of hard sweep. Grey box: expressing lines. In the TSS region there is a derived allele fixed in expressing lines but the flanking regions of expressing chromosomes retain nucleotide variation.