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.

Chemical Variation among Castes, Female Life Stages and Populations of the Facultative Eusocial Sweat Bee Halictus rubicundus (Hymenoptera: Halictidae)

“…We identified more than 50 compounds which were solely found either in the European and North American populations, including different isomers of nalkenes and macrocyclic lactones, which indicates unique odor profiles that probably arose through chemical 'drift' analogous to differentiation through genetic drift for genetic markers. As cuticular hydrocarbons and also macrocyclic lactones are mainly synthesized by the insects themselves and do not have any environmental origin (Blomquist and Bagnères 2010;Holze et al 2020;Schulz and Hötling 2015), we assume that the differences we found in cuticular chemical profiles are indeed based on genetic differences between populations. Comparable results have already been shown for different species of bumblebees (Bunk et al 2010;Martin et al 2010) or stingless bees (Martin et al 2017), in which different nalkene isomers separate different species.…”

Immune Stimulation via Wounding Alters Chemical Profiles of Adult Tribolium castaneum

“…Interestingly, we found similar results in our previous transcriptome study (Behrens et al 2014; Table S3) where we observed an upregulation of multiple candidate fatty acid synthase (FAS) genes, 6 h and 18 h post wounding in T. castaneum larvae. FASs are involved in the production of methyl alkanes (Blomquist & Ginzel, 2021;Holze et al, 2021).…”

“…Interestingly, we found similar results in our previous transcriptome study (Behrens et al 2014; Table S3) where we observed an upregulation of multiple candidate fatty acid synthase (FAS) genes, 6 h and 18 h post wounding in T. castaneum larvae. FASs are involved in the production of methyl alkanes (Blomquist & Ginzel, 2021; Holze et al, 2021). In comparison to n -alkanes (linear alkanes), methyl alkanes were shown to be more important in cue recognition (reviewed in van Zweden & d’Ettorre, 2010) and to mediate detection of T. castaneum larvae by parasitoids (Awater-Salendo et al, 2020).…”

Modulation of fatty acid elongation sustains sexually dimorphic hydrocarbons and female attractiveness inBlattella germanica(L.)

“…The diversity of HCs in insects is reflected in the HC carbon chain lengths, their degree of saturation, and the number and positions of methyl groups (Holze et al, 2020). HCs in B. germanica are composed of only alkanes and methyl-branched alkanes, and the fatty acid biosynthesis gene that governs the incorporation of methyl groups in the aliphatic chain showed no role in generating the sexual dimorphism of HCs in B. germanica (Pei et al, 2019).…”

“…The VLCF acyl-CoAs are finally reduced to long-chain alcohols by fatty acyl-CoA reductases (FARs) and converted to HCs by the P450 oxidative decarbonylase CYP4Gs (Qiu et al, 2012; MacLean et al, 2018; Li et al, 2019a). It is now clear that the variation in CHCs is primarily reflected in the chain length, number and positions of methyl groups, and the degree of unsaturation, which are determined by ELOs, FASs, and Desats, respectively (Blomquist and Bagnères, 2010; Chung and Carroll, 2015; Holze et al, 2020). These genes have been studied in few insect species with regard to SDHCs.…”