Patterns of transcriptional parallelism and variation in the developing olfactory system of Drosophila species

Abstract

Organisms have evolved strikingly parallel phenotypes in response to similar selection pressures suggesting that there may be shared constraints limiting the possible evolutionary trajectories. For example, the behavioral adaptation of specialist Drosophila species to specific host plants can exhibit parallel changes in their adult olfactory neuroanatomy. We investigated the genetic basis of these parallel changes by comparing gene expression during the development of the olfactory system of two specialist Drosophila species to that of four other generalist species. Our results suggest that the parallelism observed in the adult olfactory neuroanatomy of ecological specialists extends more broadly to their developmental antennal expression profiles, and to the transcription factor combinations specifying olfactory receptor neuron (ORN) fates. Additionally, comparing general patterns of variation for the antennal transcriptional profiles in the adult and developing olfactory system of the six species suggest the possibility that specific, non-random components of the developmental programs underlying the Drosophila olfactory system harbor a disproportionate amount of interspecies variation. Further examination of these developmental components may be able to inform a deeper understanding of how traits evolve.

Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit

“…Interestingly, these receptors also appear to have important functions. Or33a has unknown function [25], but like Or22a, it shows variable expression across species [26]. Or67a detects aromatic esters (e.g., methyl benzoate) [27] and has undergone serial duplication in Drosophila suzukii and Drosophila biarmipes [28].…”

Functional Interaction Between Drosophila Olfactory Sensory Neurons and Their Support Cells

“…However, one cannot exclude that support cells are directly connected between each other via gap junctions, or that a subset of sensilla may harbor neuronsupport cell junctions and channels. Indeed, this may be a likely possibility given that the expression of insect gap junction proteins, namely the innexins ogre/inx1, inx2, and inx3, are expressed in substantial levels in adult fly antennae as surveyed by several independent studies employing antennal tissue RNA-seq (Shiao et al, 2013;Menuz et al, 2014;Barish et al, 2017;Pan et al, 2017). Innexins in adult insect sensory systems have hitherto only been described in the auditory system, where they are involved in the synaptic coupling between auditory sensory neurons and the giant fiber (Pézier et al, 2016), but have been tentatively noted in early silk moth EM studies looking at membrane-to-membrane contacts (Steinbrecht, 1980).…”

Olfactory Receptor Gene Regulation in Insects: Multiple Mechanisms for Singular Expression

“…Knowledge of the timing of olfactory receptor expression is critical to distinguish if developmental regulators have direct or indirect roles in inducing receptor gene transcription. Recent antennal bulk and single-cell/nuclear OSN RNA-sequencing at multiple timepoints indicates that transcripts for a subset of receptors are first detected from ∼24 h after puparium formation ( Pan et al, 2017 ; Li et al, 2020 ; McLaughlin et al, 2021 ), at most a few hours after the terminal division of these lineages ( Endo et al, 2011 ; Chai et al, 2019 ). Other receptors initiate expression over the subsequent ∼24–48 h, potentially reflecting asynchrony in SOP lineage development and/or differences in the mechanisms/levels of transcriptional induction.…”

“…The overall precision of olfactory receptor expression within a species belies the flexibility of this sensory system over evolutionary timescales ( Ramdya and Benton, 2010 ). Comparative antennal transcriptomic studies (using bulk RNA-sequencing) in closely related species have revealed differences in expression level of many receptors ( McBride et al, 2014 ; Shiao et al, 2015 ; Crowley-Gall et al, 2016 ; Pan et al, 2017 ), although these datasets cannot distinguish changes in receptor expression level within an OSN population from changes in numbers of neurons expressing a particular gene. More strikingly, enormous variation exists in the size of olfactory receptor repertoires (from <10 to >500) – and, presumably, corresponding number of neuron types – between species ( Robertson, 2019 ; Yan et al, 2020 ).…”