Formation and Longevity of Chimeric and Duplicate Genes inDrosophila melanogaster

Abstract

Historically, duplicate genes have been regarded as a major source of novel genetic material. However, recent work suggests that chimeric genes formed through the fusion of pieces of different genes may also contribute to the evolution of novel functions. To compare the contribution of chimeric and duplicate genes to genome evolution, we measured their prevalence and persistence within Drosophila melanogaster. We find that $80.4 duplicates form per million years, but most are rapidly eliminated from the genome, leaving only 4.1% to be preserved by natural selection. Chimeras form at a comparatively modest rate of $11.4 per million years but follow a similar pattern of decay, with ultimately only 1.4% of chimeras preserved. We propose two mechanisms of chimeric gene formation, which rely entirely on local, DNA-based mutations to explain the structure and placement of the youngest chimeric genes observed. One involves imprecise excision of an unpaired duplication during large-loop mismatch repair, while the other invokes a process akin to replication slippage to form a chimeric gene in a single event. Our results paint a dynamic picture of both chimeras and duplicate genes within the genome and suggest that chimeric genes contribute substantially to genomic novelty.

Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross

“…Overall, most chimeras of maternal/paternal origin do not overlap, and this phenomenon indicates nonreciprocal structural change. Chimeric genes might have formed after the two genomes merged and before whole genome duplication that leads to tetraploidization (46). Both chimeric genes and nonsynonymous mutations might produce structural changes that reduce enzyme activity or fidelity by affecting normal transcriptional processing (47).…”

“…The high frequency of chimeras and mutation also might result from largescale DNA repair via recombination or nonhomologous end-joining, or even transposon activity (48)(49)(50)(51). The common occurrence of chimeric genes that persists throughout the initial 22 generations of hybrid fishes might result from different processes that relate to chimeras: replication slippage or the imprecise cutting of an unpaired duplication during large-loop mismatch repair (46). Abnormalities of DNA or RNA repair, such as dysfunction of RAD (52, 53) or other genes and pathways (e.g., UBE2N/UBC13, ssb in Datasets S1 and S2 and SI Appendix, Fig.…”

Functional Copies of the Mst77F Gene on the Y Chromosome of Drosophila melanogaster

“…The timescale of these events is an important issue here, but unfortunately it is poorly known. Depending on which estimate of the half-life of Drosophila duplicate genes we use [0.66 MY (Rogers et al 2009) zation such as presence of frameshift or nonsense mutations. Among the remaining 8 Mst77Y genes, while we cannot exclude the possibility of neofunctionalization, the observation that they are expressed in the same organ (testis) suggests that they have the same function of the parental gene Mst77F.…”

Adaptive impact of the chimeric gene Quetzalcoatl in Drosophila melanogaster

“…Such rearrangements can produce novel combinations of existing modular elements, contributing to the development of genes with novel functions (1). Chimeric genes appear to be common in the genomes of multicellular organisms, including humans (2)(3)(4)(5). They are formed often in Drosophila melanogaster (5,6), and there are several known examples of chimeric genes that have been stably incorporated into the genome (5).…”

“…Chimeric genes appear to be common in the genomes of multicellular organisms, including humans (2)(3)(4)(5). They are formed often in Drosophila melanogaster (5,6), and there are several known examples of chimeric genes that have been stably incorporated into the genome (5). Although a handful of chimeric genes shows signatures of positive selection in Drosophila (7)(8)(9)(10)(11)(12), there are very few with known functions, and the factors influencing the physiological and evolutionary impacts of chimeric genes are largely unknown.…”