Functional and molecular evolution of olfactory neurons and receptors for aliphatic esters across the Drosophila genus

Abstract

Insect olfactory receptor (Or) genes are large, rapidly evolving gene families of considerable interest for evolutionary studies. They determine the responses of sensory neurons which mediate critical behaviours and ecological adaptations. We investigated the evolution across the genus Drosophila of a subfamily of Or genes largely responsible for the perception of ecologically relevant aliphatic esters; products of yeast fermentation and fruits. Odour responses were recorded from eight classes of olfactory receptor neurons known to express this Or subfamily in D. melanogaster and from homologous sensilla in seven other species. Despite the fact that these species have diverged over an estimated 40 million years, we find that odour specificity is largely maintained in seven of the eight species. In contrast, we observe extensive changes in most neurons of the outgroup species D. virilis, and in two neurons across the entire genus. Some neurons show small shifts in specificity, whilst some dramatic changes correlate with gene duplication or loss. An olfactory receptor neuron response similarity tree did not match an Or sequence similarity tree, but by aligning Or proteins of likely functional equivalence we identify residues that may be relevant for odour specificity. This will inform future structure-function studies of Drosophila Ors.

Population differences in olfaction accompany host shift in Drosophila mojavensis

“…Seven ORNs showed no significant population differences in their response properties ( figure 1a,b). This high level of conservation in five of the seven ORNs is in line with our understanding from D. melanogaster that they function as general detectors of habitat suitability, for instance, as a general yeast detector (ab1A, ab2A, ab7B, pb2B and pb3B [28,38,39]). The receptors of the remaining two ORNs are unknown.…”

“…Having established this within D. mojavensis, we used the mean responses of these subtypes in a cluster analysis with recordings of known D. melanogaster subtypes. This reveals that the three large antennal basiconic (ab) subtypes (Dmojab1 -3) were highly similar in their response properties to their D. melanogaster equivalent (figure 1a; electronic supplementary material, figure S2, [9,18,26,28] Other ORNs did not, and these responses fell into two categories: (i) ORNs previously shown to have high variability among drosophilid species [28,35,38,39] or (ii) ORNs in which the corresponding receptor is not bioinformatically predicted to be present in D. mojavensis [35]. The remaining three, DmojabX -Z, could not be unambiguously matched by their responses to known D. melanogaster subtypes.…”

“…This sensitivity for aromatics has not been shown for the four basiconic receptors significantly upregulated in the S. Catalina population. These receptors have been shown to be sensitive to esters (figure 1a,b, [28]). Thus, the physiological differences between populations of this species appear to be reflected in, and likely derived from, the molecular machinery and reflective of their host plant use.…”

Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet

“…The OR family has been functionally annotated in D. melanogaster (reviewed in ref. 28), and members of subfamily H OR genes in particular (20) are highly conserved and enriched in receptors for aliphatic esters (35), a group of compounds S. flava detected poorly.…”

Olfactory coding in five moth species from two families

“…Recent comparative studies revealed OSNs with mainly conserved receptive ranges or conserved representation patterns of odorants in the first olfactory neuropil across species, with only little impact of speciesspecific life histories. In these studies, however, only species belonging to the same family [Nymphalidae (Carlsson et al, 2011;Ômura and Honda, 2009)], subfamily [Heliothinae (Rostelien et al, 2005;Stranden et al, 2003); Murinae (Johnson et al, 2009;Soucy et al, 2009)], or genus [Drosophila (de Bruyne et al, 2010;Stensmyr et al, 2003)] were investigated. Remarkable similarities in olfactory coding were also found across the ant Camponotus fellah, the bee Apis mellifera and the rat Rattus norvegicus, i.e.…”