Birth-and-Death Evolution of the Fatty Acyl-CoA Reductase (FAR) Gene Family and Diversification of Cuticular Hydrocarbon Synthesis in Drosophila

Abstract

The birth-and-death evolutionary model proposes that some members of a multigene family are phylogenetically stable and persist as a single copy over time, whereas other members are phylogenetically unstable and undergo frequent duplication and loss. Functional studies suggest that stable genes are likely to encode essential functions, whereas rapidly evolving genes reflect phenotypic differences in traits that diverge rapidly among species. One such class of rapidly diverging traits are insect cuticular hydrocarbons (CHCs), which play dual roles in chemical communications as short-range recognition pheromones as well as protecting the insect from desiccation. Insect CHCs diverge rapidly between related species leading to ecological adaptation and/or reproductive isolation. Because the CHC and essential fatty acid biosynthetic pathways share common genes, we hypothesized that genes involved in the synthesis of CHCs would be evolutionary unstable, whereas those involved in fatty acid-associated essential functions would be evolutionary stable. To test this hypothesis, we investigated the evolutionary history of the fatty acyl-CoA reductases (FARs) gene family that encodes enzymes in CHC synthesis. We compiled a unique data set of 200 FAR proteins across 12 Drosophila species. We uncovered a broad diversity in FAR content which is generated by gene duplications, subsequent gene losses, and alternative splicing. We also show that FARs expressed in oenocytes and presumably involved in CHC synthesis are more unstable than FARs from other tissues. Taken together, our study provides empirical evidence that a comparative approach investigating the birth-and-death evolution of gene families can identify candidate genes involved in rapidly diverging traits between species.

Large-scale characterization of sex pheromone communication systems inDrosophila

“…The observed saltational changes are not necessarily unexpected as minor mutations suffice to induce large-scale changes in the biosynthetic pathways of sex pheromones 66,73,74 . Likewise, gene families involved in biosynthesis of cuticular chemicals have been shown to evolve rapidly and independently among closely related drosophilids 75 .…”

Molecular evolution of gland cell types and chemical interactions in animals

“…They are produced by primary metabolism of sugars and converted into aldehydes or alcohols by FACRs. A dedicated oenocyte FACR converts fattyacyl-CoA into an aldehyde precursor for insect CHCs (Cinnamon et al, 2016;Finet et al, 2019;Jaspers et al, 2014). Species-specific FACRs are expressed in female moth sex pheromone glands, where they produce fatty alcohols for conversion into acetate pheromones (Carot-Sans et al, 2015;Hagström et al, 2013;Lassance et al, 2010;Liénard et al, 2010;Moto et al, 2003).…”

“…However, there is an apparent counter to this process, evident in pervasive convergence in the types of compounds animals synthesize. Convergence is seen in the widespread use of fatty-acid-derived compounds like hydrocarbons and alcohols for chemical communication (Blomquist and Bagneres, 2010;Chung and Carroll, 2015;Finet et al, 2019;Leonhardt et al, 2016;Morgan, 2010;Tegoni et al, 2004) or the employment of terpenes for diverse processes (Beran et al, 2019;Blunt et al, 2014;Breitmaier, 2006;Trapp and Croteau, 2001). A further example is the frequent use of aromatic benzoquinones for chemical defensive; these compounds have evolved repeatedly in harvestman, millipedes, earwigs, crickets, termites, cockroaches, caddisflies and at least four different families of beetles (Blum, 1981;Eisner et al, 2005;Francke and Dettner, 2005).…”

Climate change and the genetics of insecticide resistance

“…CHCs are synthesized in specialized oenocyte cells via the fatty acyl-CoA synthesis pathway involving a series of fatty acyl-CoA modification enzymes such as desaturases, elongases, and reductases that metabolize acetyl-CoA to alcohols and aldehydes before the final decarbonylation to long-chained hydrocarbons by a CYP4G cytochrome P450 enzyme. 34,35 Removing all CHCs by RNA interference (RNAi) knockdown of this CYP4G ortholog in D. melanogaster, Cyp4g1, resulted in severe desiccation sensitivity in D. melanogaster. 35 Variations in the composition and levels of CHCs between insects have also been positively associated with differences in desiccation resistance.…”

“…The layer of waxy cuticular hydrocarbons (CHCs), the outermost hydrophobic layer on the insect body surface, has an important role in controlling water loss by reducing the rate of evaporation through the cuticle. CHCs are synthesized in specialized oenocyte cells via the fatty acyl‐CoA synthesis pathway involving a series of fatty acyl‐CoA modification enzymes such as desaturases, elongases, and reductases that metabolize acetyl‐CoA to alcohols and aldehydes before the final decarbonylation to long‐chained hydrocarbons by a CYP4G cytochrome P450 enzyme . Removing all CHCs by RNA interference (RNAi) knockdown of this CYP4G ortholog in D. melanogaster , Cyp4g1 , resulted in severe desiccation sensitivity in D. melanogaster .…”