  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.
