Little qualitative RNA misexpression in sterile male F1 hybrids of Drosophila pseudoobscura and D. persimilis

Abstract

Background: Although the genetics of hybrid sterility has been the subject of evolutionary studies for over sixty years, no one has shown the reason(s) why alleles that operate normally within species fail to function in another genetic background. Several lines of evidence suggest that failures in normal gene transcription contribute to hybrid dysfunctions, but genome-wide studies of gene expression in pure-species and hybrids have not been undertaken. Here, we study genome-wide patterns of expression in Drosophila pseudoobscura, D. persimilis, and their sterile F1 hybrid males using differential display.

Results: Over five thousand amplifications were analyzed, and 3312 were present in amplifications from both of the pure species. Of these, 28 (0.5%) were not present in amplifications from adult F1 hybrid males. Using product-specific primers, we were able to confirm one of nine of the transcripts putatively misexpressed in hybrids. This transcript was shown to be male-specific, but without detectable homology to D. melanogaster sequence.

Conclusion: We tentatively conclude that hybrid sterility can evolve without widespread, qualitative misexpression of transcripts in species hybrids. We suggest that, if more misexpression exists in sterile hybrids, it is likely to be quantitative, tissue-specific, and/ or limited to earlier developmental stages. Although several caveats apply, this study was a first attempt to determine the mechanistic basis of hybrid sterility, and one potential candidate gene has been identified for further study.

Figure 1

PCRs of transcript putatively misexpressed in hybrids (tmh) and a positive control (Adh). Upper lanes are, form the far left, 100-bp ladder, tmh from male D. persimilis cDNA, tmh from male D. pseudoobscura cDNA, tmh from male F₁ hybrid cDNA, tmh from female D. persimilis cDNA, tmh from female D. pseudoobscura cDNA, tmh from female F₁ hybrid cDNA, negative control of tmh PCR, tmh from D. persimilis genomic DNA, tmh from D. pseudoobscura genomic DNA. The lower nine lanes are as above but of Adh rather than tmh.