Advances in deciphering the genetic basis of insect cuticular hydrocarbon biosynthesis and variation

Abstract

Cuticular hydrocarbons (CHCs) have two fundamental functions in insects. They protect terrestrial insects against desiccation and serve as signaling molecules in a wide variety of chemical communication systems. It has been hypothesized that these pivotal dual traits for adaptation to both desiccation and signaling have contributed to the considerable evolutionary success of insects. CHCs have been extensively studied concerning their variation, behavioral impact, physiological properties, and chemical compositions. However, our understanding of the genetic underpinnings of CHC biosynthesis has remained limited and mostly biased towards one particular model organism (Drosophila). This rather narrow focus has hampered the establishment of a comprehensive view of CHC genetics across wider phylogenetic boundaries. This review attempts to integrate new insights and recent knowledge gained in the genetics of CHC biosynthesis, which is just beginning to incorporate work on more insect taxa beyond Drosophila. It is intended to provide a stepping stone towards a wider and more general understanding of the genetic mechanisms that gave rise to the astonishing diversity of CHC compounds across different insect taxa. Further research in this field is encouraged to aim at better discriminating conserved versus taxon-specific genetic elements underlying CHC variation. This will be instrumental in greatly expanding our knowledge of the origins and variation of genes governing the biosynthesis of these crucial phenotypic traits that have greatly impacted insect behavior, physiology, and evolution.

Fig. 1. Right: Schematic insect, middle: Cross-section through its integument highlighting CHC transport pathways and their deposition on the epicuticle, left: examples of the three most commonly occurring CHC compound classes n-alkanes, n-alkenes, and methyl-branched alkanes.

CHC biosynthesis occurs in specialized secretory cells, the oenocytes, which are mainly embedded in clusters in the epidermis or dispersed within the fat body depending on insect species and developmental stage. After their biosynthesis, CHCs are shuttled through the hemolymph by the high-density lipoprotein lipophorin, with subsequent transport to the epicuticular surface via specialized pore canals penetrating the cuticular layers. Gray arrows indicate CHC transport pathways, drawings by Lukas Schrader.

Fig. 2. Schematic summary of the current state of knowledge for the CHC biosynthesis pathway in insects.

Circles designate chemical compounds, rectangles the corresponding enzymes catalyzing their transitions. Enzymes are numbered from 1 to 10 according to their hypothesized order in the pathway, and asterisks correspond to the respective number of characterized genes whose depicted function has been empirically demonstrated through targeted knockdown studies listed in Table 1. Reactions and interactions in the CHC biosynthesis pathway that are not completely understood are marked with dashed arrows and question marks. Acetyl-CoA as the initial reactant of CHC biosynthesis is mainly provided by the citric acid cycle. Note that the distinction between microsomal and cytosolic fatty acid synthase is hypothetical and has not yet been unambiguously confirmed. Abbreviations: CoA: Coenzyme A, ACC: acetyl-CoA carboxylase, MCD: malonyl-CoA decarboxylase, LaAT: lipoamide acyltransferase, LCF(A): long-chain fatty (acid), VLC(F): very-long chain (fatty), mb: methyl-branched, un: unsaturated. Figure adapted and synthesized from Howard and Blomquist (2005), Blomquist and Bagnères (2010), Chung and Carroll (2015), Ginzel and Blomquist (2016).