Gap genes are involved in inviability in hybrids between Drosophila melanogaster and D. santomea

Abstract

Evolved changes within species can lead to the loss of viability in hybrids. Inviability is also a convenient phenotype to genetically map and validate functionally divergent genes and pathways differentiating closely related species. Here, I identify the Drosophila melanogaster form of the highly conserved essential gap gene giant (gt) as a key genetic determinant of inviability in hybrids with D. santomea. The presence of this allele is sufficient and necessary to cause a prevalent abdominal ablation in the developing hybrid embryo. Further genetic analysis indicates that tailless (tll), another gap gene, is also involved in the hybrid defects. giant and tll are both members of the gap gene network of transcription factors that participate in establishing anterior-posterior specification of the dipteran embryo, a highly conserved developmental process. I found no evidence for positive selection in either of the two genes. Genes whose outputs in this process are functionally conserved nevertheless evolve over short timescales to cause inviability in hybrids. SIGNIFICANCE STATEMENTHybrid organisms--which have parents from different species--are usually less healthy than pure-species organisms. Hybrid inviability is an extreme example of this phenomenon. Defects result from incompatibilities between genes that have diverged in the parental species. In this piece, I dissect the genetic basis of hybrid inviability between two species of Drosophila: D. melanogaster and D. santomea. I identified two genes, gt and tll responsible for the inviability in these hybrids. The two genes belong to the gap gene network, a highly conserved pathway that is in charge of establishing embryonic polarity in insects. These results show that developmentally important genes might evolve sufficiently fast to cause hybrid inviability in species that still can interbreed.