Species and sex-specific chemosensory gene expression in Anopheles coluzzii and An. quadriannulatus antennae

Abstract

Background: Olfactory cues drive mosquito behaviors such as host-seeking, locating sugar sources and oviposition. These behaviors can vary between sexes and closely related species. For example, the malaria vector Anopheles coluzzii is highly anthropophilic, whereas An. quadriannulatus is not. These behavioral differences may be reflected in chemosensory gene expression. Methods: The expression of chemosensory genes in the antennae of both sexes of An. coluzzii and An. quadriannulatus was compared using RNA-seq. The sex-biased expression of several genes in An. coluzzii was also compared using qPCR. Results: The chemosensory expression is mostly similar in the male antennae of An. coluzzii and An. quadriannulatus, with only a few modest differences in expression. A handful of chemosensory genes are male-biased in both species; the highly expressed gustatory receptor AgGr33, odorant binding proteins AgObp25, AgObp26 and possibly AgObp10. Although the chemosensory gene repertoire is mostly shared between the sexes, several highly female-biased AgOrs, AgIrs, and one AgObp were identified, including several whose expression is biased towards the anthropophilic An. coluzzii. Additionally, the expression of several chemosensory genes is biased towards An. coluzzii in both sexes. Conclusions: Chemosensory gene expression is broadly similar between species and sexes, but several sex-biased/ specific genes were identified. These may modulate sex-and species-specific behaviors. Although the male behavior of these species remains poorly studied, the identification of sex-and species-specific chemosensory genes may provide fertile ground for future work.

The Expression of Chemosensory Genes in Male Maxillary Palps ofAnopheles coluzzii(Diptera: Culicidae) andAn. quadriannulatus

“…In contrast to the male antennae ( Athrey et al 2020 ), no chemosensory genes in the palps were male-specific in these species, i.e., all the genes expressed in males are expressed in females as well ( Pitts et al 2011 , Athrey et al 2017 ). However, several chemosensory genes were species-specific when comparing An.…”

“…coluzzii and zoophilic An. quadriannulatus ( Pitts et al 2011 , Rinker et al 2013 , Athrey et al 2017 , Saveer et al 2018 , Athrey et al 2020 ). Here, we extended that work by comparing chemosensory gene expression in the male maxillary palps of these two species.…”

“…coluzzii exceeds that of all other chemoreceptors and the expression of this gene is also exclusive or highly biased towards An. coluzzii in male and female antennae, as well as female palps ( Athrey et al 2020 ). Furthermore, the labella of both sexes of An.…”

“…coluzzii and An. quadriannulatus express the gustatory receptor Gr33 in their antennae at high levels, whereas this receptor is all but absent in female antennae ( Pitts et al 2011 , Athrey et al 2020 ). It is tempting to speculate that it plays a role in mating behavior, either during swarm formation or recognition of conspecific females.…”

Interpopulational Variations of Odorant-Binding Protein Expression in the Black Cutworm Moth, Agrotis ipsilon

“…Natural genetic variation also likely contributes to reprogramming of olfactory receptor neurons and odor choice, as described in the worm Caenorhabditis elegans [ 88 , 89 ]. However, the detection of differing odor sources by sibling species in moths may be reflected not only in the memorization of specific olfactory signals and new assemblies of integrative networks in the brain, but also in the expression level of the various olfactory genes involved in peripheral organs such as the antennae [ 90 , 91 ]. It has been shown that the acclimation to specific environmental cues requires gene transcriptional variations in olfactory receptor organs [ 92 ].…”