New gene formation in hybrid Drosophila

TL;DR

This study reveals a novel mechanism of new gene creation in hybrid Drosophila, driven by epistatic interactions during hybridization, leading to rapid genetic novelty without new mutations.

Contribution

It uncovers a new model of gene formation in hybrids that relies on epistatic interactions, not DNA mutations, expanding understanding of genetic innovation.

Findings

Bursts of new gene creation observed in hybrid Drosophila.

Asymmetry in gene creation based on cross direction.

Activation of silenced alleles from one parent by the other.

Abstract

The origin of new genes is among the most fundamental processes underlying genetic innovation. The substrate of new genetic material available defines the outcomes of evolutionary processes in nature. Historically, the field of genetic novelty has commonly invoked new mutations at the DNA level to explain the ways that new genes might originate. In this work, we explore a fundamentally different source of epistatic interactions that can create new gene sequences in hybrids. We observe "bursts" of new gene creation in F1 hybrids of D. yakuba and D. santomea, a species complex known to hybridize in nature. The number of new genes is higher in the gonads than soma. We observe asymmetry in new gene creation based on the direction of the cross. Greater numbers of new transcripts form in the testes of F1 male offspring in D. santomea female x D. yakuba male crosses and greater numbers of new transcripts appear in ovaries of F1 female offspring of D. yakuba female x D. santomea male. These loci represent wholly new transcripts expressed in hybrids, but not in either parental reference strain of the cross. We further observe allelic activation, where transcripts silenced in one lineage are activated by the transcriptional machinery of the other genome. These results point to a fundamentally new model of new gene creation that does not rely on the formation of new mutations in the DNA. These results suggest that bursts of genetic novelty can appear in response to hybridization or introgression in a single generation. Ultimately these processes are expected to contribute to the substrate of genetic novelty available in nature, with broad impacts on our understanding new gene formation and on hybrid phenotypes in nature.