Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

Abstract

The insect odorant receptor (Or) gene family is among the largest multigene families in insect genomes, but its evolutionary origin and mode of expansion is still a matter of debate. We performed transcriptomic surveys of two wingless insect species, the silverfish Lepisma saccharina and Tricholepidion gertschi, and identified multiple Or gene family members in both species. A phylogenetic analysis suggests that the silverfish Ors do not fall into the clade comprised of more derived flying insect ligand-binding Ors, but, along with bristletail, firebrat and some mayfly Ors, are consistently resolved as a distinct set of genes that may constitute an evolutionary intermediate between gustatory receptors and the more derived Ors of flying insects. We propose to consider these "primitive Ors" separately from higher insect Ors until their cellular expression patterns and function are resolved and suggest a multistep evolutionary scenario ultimately leading to the highly sensitive, rapidly evolving and physiologically diverse Or gene family observed in higher insects.

Functional properties of insect olfactory receptors: ionotropic receptors and odorant receptors

“…While OR genes were absent in non-insect hexapods such as springtails, they were found in winged and non-winged insects ( Brand et al 2018). According to a phylogenetic analysis of OR genes there is an intermediate clade of primitive ORs expressed in bristletails, firebrats, or silverfish between GRs and the ORs of flying insects (Thoma et al 2019). These primitive ORs then disappeared in flying insects, e.g., in damselflies and dragonflies.…”

“…The current state of knowledge supports the view that the ORs evolved from the GRs in a stepwise process. Starting with primitive ORs in early terrestrial insects (Thoma et al 2019), the olfactory system has expanded its receptor repertoire with the occurrence of Orco proteins in Zygentoma (Brand et al 2018) and ended up with the versatile OR complexes in flying insects (Brand et al 2018;Thoma et al 2019) (Fig. 2c).…”

“…The emergence of ORs pre-dates the evolution of winged insects (Pterygota) and OR genes have been detected in basal insects. The conserved olfactory receptor-coreceptor (Orco) has not been detected in Archaeognatha and may be evolved later or being lost in this Order (Brand et al 2018 ; Thoma et al 2019 ). Winged insects show a huge expansion in their number of OR genes (blue triangle) …”

“…These primitive ORs then disappeared in flying insects, e.g., in damselflies and dragonflies. Furthermore, in winged insects there was a massive expansion of OR genes (Missbach et al 2014 ; Thoma et al 2019 ). These ORs are heteromeric constructs containing variable, odor-specific OrX proteins, and highly conserved co-receptor proteins (Orco) (Larsson, et al 2004 ; Neuhaus et al 2005 ; Soffan et al 2018 ).…”

Adaptive evolution of olfactory degeneration in recently flightless insects

“…Missbach et al (14) suggested that the OR/Orco system represents a specific adaptation associated with insect flight (but see (13) for an opposing view). While OR genes likely evolved in the common ancestor of modern insects, perhaps as an adaptation to terrestrial conditions (13, 25), the OR/Orco system may have arisen more recently (15). Indeed, the fact that genomes of early-diverging (non-flying) insect lineages, such as jumping bristletails (Archaeognatha), have ORs but not Orco, suggests the OR/Orco system has a later origin and facilitates rapid olfaction in winged insects (15).…”