Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans - PubMed (original) (raw)
Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans
José M Ranz et al. Genome Res. 2004 Mar.
Abstract
When females of Drosophila melanogaster and males of Drosophila simulans are mated, the male progeny are inviable, whereas the female progeny display manifold malformations and are sterile. These abnormalities result from genetic incompatibilities accumulated since the time the lineages of the species diverged, and may have their origin in aberrant gene transcription. Because compensatory changes within species may obscure differences at the regulatory level in conventional comparisons of the expression profile between species, we have compared the gene-expression profile of hybrid females with those of females of the parental species in order to identify regulatory incompatibilities. In the hybrid females, we find abnormal levels of messenger RNA for a large fraction of the Drosophila transcriptome. These include a gross underexpression of genes preferentially expressed in females, accompanying gonadal atrophy. The hybrid females also show significant overexpression of male-biased genes, which we attribute to incompatibilities in the regulatory mechanisms that normally act to control the expression of these genes in females. The net result of the multiple incompatibilities is that the gene-expression profiles of the parental females are more similar to each other than either is to that of the hybrid.
Figures
Figure 1
Set of competitive hybridizations onto cDNA microarrays performed to compare the expression profile among D. melanogaster, D. simulans, and hybrid females. Twenty-one hybridizations were carried out with mRNA from whole flies (solid arrows) and 12 with head-specific amplified mRNA (dashed arrows). Arrowhead, sample labeled with Cy5; base of arrow, sample labeled with Cy3. Each comparison was replicated six times for whole-fly mRNA and four times for head mRNA. Three self-self hybridizations were also carried out for the whole-body experiment. The resulting experimental design was balanced for dyes and samples.
Figure 2
Classification of the cDNAs assayed according to the relationships at expression level among D. melanogaster (red), D. simulans (blue), and hybrid (green) in whole-body (orange cells) and heads only (yellow cells) experiments. Only the 4450 array elements regarded as consistent with the Bayesian methodology (Townsend and Hartl 2002) in the whole-body analysis have been included (Methods); in the case of the experiments with head mRNA, no reliable estimate was obtained by Bagel for two of the 4450 array elements considered. The logical operators (=, <, >) denote the relationship among the 95% credible intervals of the mean expression levels obtained for the three kind of females. The number that appears in a particular cell shows the total number of genes on our cDNA microarray that meet the three different conditions under which each gene can be classified. The eight empty cells correspond to mutually incompatible requirements. See Supplemental Figure 2 for numerical code of the cells in orange.
Figure 3
Hierarchical clustering of the mean levels of expressions estimated using a Bayesian methodology (BAGEL) for the whole-body experiments. Underexpressed genes (blue); overexpressed genes (red). Ward's minimum variance was used as a distance metric. The dendrogram includes 3965 genes that showed significantly different expression levels in at least one of the three pairwise comparisons between females. (mel) D. melanogaster; (sim) D. simulans; (hyb) hybrid.
Figure 4
Patterns of misregulation between hybrids and females of D. melanogaster and D. simulans in whole-body experiments. (A) orb, a gene underexpressed in the hybrid and required for correct oogenesis in a normal female. (B) Adh, a gene overexpressed in the hybrid that is highly expressed in the fat body (Dickinson et al. 1984). (C) dream, a gene for which the allele of D. melanogaster is dominant over that of D. simulans, which involves a higher level of expression. (D) sxe2, a gene overexpressed in the hybrid that is expressed in the brain of males only (Fujii and Amrein 2002). Female symbol subscripts indicate the genotype; (m) D. melanogaster; (s) D. simulans; (h) hybrid. Error bars indicate the 95% credible intervals around the estimated mean expression level. Three pairwise comparisons are possible among the three female genotypes. Differences in level of gene expression are regarded to be statistically significant if the 95% credible intervals of the estimates failed to overlap. (=) No significant difference; (>) significant overexpression.
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References
- Arbeitman, M.N., Furlong, E.E., Iman, F., Johnson, E., Null, B.H., Baker, B.S., Krasnow, M.A., Scott, M.P., and White, K.P. 2002. Gene expression during the life cycle of Drosophila melanogaster. Science 297: 2270–2275. - PubMed
- Bonnier, G. 1924. Contributions to the knowledge of intra- and interspecific relationships in Drosophila. Acta Zool. 5: 1–122.
- Carson, H.L. 1985. Unification of speciation theory in plants and animals. Syst. Bot. 10: 380–390.
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