Molecular Evolution and Functional Diversification of Fatty Acid Desaturases after Recurrent Gene Duplication in Drosophila

Abstract

Frequent gene duplications in the genome incessantly supply new genetic materials for functional innovation presumably driven by positive Darwinian selection. This mechanism in the desaturase gene family has been proposed to be important in triggering the pheromonal diversification in insects. With the recent completion of a dozen Drosophila genomes, a genome-wide perspective is possible. In this study, we first identified homologs of desaturase genes in 12 Drosophila species and noted that while gene duplication events are relatively frequent, gene losses are not scarce, especially in the desat1–desat2–desatF clade. By reconciling the gene tree with species phylogeny and the chromosomal synteny of the sequenced Drosophila genomes, at least one gene loss in desat2 and a minimum of six gene gains (resulting in seven desatF homologs, α-η), three gene losses and one relocation in desatF were inferred. Upon branching off the ancestral desat1 lineage, both desat2 and desatF gained novel functions through accelerating protein evolution. The amino acid residues under positive selection located near the catalytic sites and the C-terminal region might be responsible for altered substrate selectivity between closely related species. The association between the expression pattern of desatF-α and the chemical composition of cuticular hydrocarbons implies that the ancestral function of desatF-α is the second desaturation at the four carbons after the first double bond in diene synthesis, and the shift from bisexual to female-specific expression in desatF-α occurred in the ancestral lineage of Drosophila melanogaster subgroup. A relationship between the number of expressed desatF homologs and the diene diversification has also been observed. These results suggest that the molecular diversification of fatty acid desaturases after recurrent gene duplication plays an important role in pheromonal diversity in Drosophila.

Loss of Drosophila pheromone reverses its role in sexual communication in Drosophila suzukii

“…B 282: 20143018 material, figure S1c,d). We note that D. suzukii and D. biarmipes lacked the desaturase desat2 and the elongases eloF, which have been implied in the biosynthesis of species-specific and sexually dimorphic CH profiles in Drosophila ( [28,29]; electronic supplementary material, figure S2). However, more striking was the lack of cVA in the chemical profile of D. suzukii (figure 1a, arrow, verified with D. suzukii from the USA: electronic supplementary material, figure S1d).…”

desat1

“…37 This suggests that the desat genes underlying pheromonal communication system have rapidely evolved. 45,46 This concerns the desat1 and desat2 genes which are located in tandem (4 kb apart) in the D. melanogaster genome (Fig. 1).…”

Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria

“…As Elovl4 proteins are responsible for elongating PUFAs, these codons may have a role in the targeting and elongating of PUFAs. A study from the genus Drosophila revealed that the Fad gene family in this group is under the influence of pervasive purifying selection but also episodic diversifying selection at specific codons (Fang et al., 2009). This study also found that the majority of the codons under episodic diversifying selection occurred in clades produced by duplication events.…”

“…Codon alignments were imported into IQ‐TREE (v1.4.2) (Nguyen et al., 2014) to determine best‐fit substitution model (GTR+I+G4), and phylogenetic trees were generated from alignments using 1,000 ultrafast bootstrap iterations. Using these alignments and phylogenetic trees as inputs, the rates of selection could be determined using maximum‐likelihood models in the program CODEML in PAML (v4.8) (Yang, 2007) using the protocol of (Fang et al., 2009) and codon frequency F3X4. To accurately determine significance, Bonferroni correction was computed to account for the repeated testing of multiple branches (Fletcher & Yang, 2010; Hunt et al., 2011) where Fad had n  = 2 branches and Elovl had n  = 4 branches and the adjusted p‐ value = .05/ n .…”