Expression Divergence of Chemosensory Genes between Drosophila sechellia and Its Sibling Species and Its Implications for Host Shift

Abstract

Drosophila sechellia relies exclusively on the fruits of Morinda citrifolia, which are toxic to most insects, including its sibling species Drosophila melanogaster and Drosophila simulans. Although several odorant binding protein (Obp) genes and olfactory receptor (Or) genes have been suggested to be associated with the D. sechellia host shift, a broad view of how chemosensory genes have contributed to this shift is still lacking. We therefore studied the transcriptomes of antennae, the main organ responsible for detecting food resource and oviposition, of D. sechellia and its two sibling species. We wanted to know whether gene expression, particularly chemosensory genes, has diverged between D. sechellia and its two sibling species. Using a very stringent definition of differential gene expression, we found a higher percentage of chemosensory genes differentially expressed in the D. sechellia lineage (7.8%) than in the D. simulans lineage (5.4%); for upregulated chemosensory genes, the percentages were 8.8% in D. sechellia and 5.2% in D. simulans. Interestingly, Obp50a exhibited the highest upregulation, an approximately 100-fold increase, and Or85c--previously reported to be a larva-specific gene--showed approximately 20-fold upregulation in D. sechellia. Furthermore, Ir84a (ionotropic receptor 84a), which has been proposed to be associated with male courtship behavior, was significantly upregulated in D. sechellia. We also found expression divergence in most of the chemosensory gene families between D. sechellia and the two sibling species. Our observations suggest that the host shift of D. sechellia was associated with the enrichment of differentially expressed, particularly upregulated, chemosensory genes.

Keywords: Drosophila sechellia; RNA-seq; antennal transcriptome; chemosensory genes; host shift.

Fig. 1.—

Venn diagrams showing genes expressed differentially in D. sechellia (Dsec) in comparing with D. melanogaster (Dmel) or D. simulans (Dsim). A total of 147 genes were significantly upregulated (A) and a total of 84 genes were significantly downregulated (B) in D. sechellia. Males and females are presented in blue and red, respectively. The 147 upregulated genes include 3 Obp genes, 6 Or genes, 1 Gr gene, 1 Ir gene, 2 CheA/B genes and 134 other genes in the transcriptome (A). The 84 downregulated genes include 3 Obp genes, 2 Or genes, and 79 other genes in the transcriptome (B).

Fig. 2.—

Heat maps of expression profiles of Or genes. (A) Heat maps of ranked expression levels of Or genes. The red color indicates the highest expression level, whereas the yellow color indicates a low expression level. Clustering results of genes is shown on the left of the figure, and the gene names and expressed sensilla (Or genes) are shown on the right. Clustering of species is shown at the top of each figure and the information of each sample is shown at the bottom of the figure. Dmel, D. melanogaster; Dsim, D. simulans; Dsec, D. sechellia; M, males; F, females; TW, Taiwan; JP, Japan. (B) Statistical significance of clustering results among three species. The approximately unbiased (au) P value (%, in red) and bootstrap probability (bp) value (%, in green) are shown on each branch (in gray color).

Fig. 3.—

Heat maps of expression profiles of Ir genes. (A) Heat maps of ranked expression levels of Ir genes and (B) statistical significance of clustering results among three species. Color patterns and sample names are as described in figure 2.

Fig. 4.—

Heat maps of expression profiles of Obp genes. (A) Heat maps of ranked expression levels of Obp genes and (B) statistical significance of clustering results among three species. Color patterns and sample names are as described in figure 2.