Modulation of odour-guided behaviour in mosquitoes

Abstract

Mosquitoes are emerging as model systems with which to study innate behaviours through neuroethology and functional genomics. Decades of work on these disease vectors have provided a solid behavioural framework describing the distinct repertoire of predominantly odour-mediated behaviours of female mosquitoes, and their dependence on life stage (intrinsic factors) and environmental cues (extrinsic factors). The purpose of this review is to provide an overview of how intrinsic factors, including adult maturation, age, nutritional status, and infection, affect the attraction to plants and feeding on plant fluids, host seeking, blood feeding, supplemental feeding behaviours, pre-oviposition behaviour, and oviposition in female mosquitoes. With the technological advancements in the recent two decades, we have gained a better understanding of which volatile organic compounds are used by mosquitoes to recognise and discriminate among various fitness-enhancing resources, and characterised their neural and molecular correlates. In this review, we present the state of the art of the peripheral olfactory system as described by the neural physiology, functional genomics, and genetics underlying the demonstrated changes in the behavioural repertoire in female mosquitoes. The review is meant as a summary introduction to the current conceptual thinking in the field.

Keywords: Host seeking; Neuroethology; Olfaction; Oviposition; Plant seeking.

Fig. 1

Diagrammatic representation of the adult female gonotrophic cycle. After eclosion, female mosquitoes share their activities amongst floral (green, medium-dashed line) and host seeking (red, solid line), and resting (yellow, short-dashed line), as shown over the first 10-day post-eclosion (dpe; top panel). After a full blood meal (solid red vertical bar), the floral and host seeking is inhibited, the latter until after oviposition (dark blue, dash-dot line), while the former is inhibited for up to 48-h post-blood meal (h pbm), when pre-oviposition behaviours (light blue, long-dashed line) begin (bottom panel). Most females oviposit within 96 h of a blood meal. The y-axis denotes the generalised proportion of mosquitoes participating in the associated behaviour based on, e.g., Alto et al. ; Bohbot et al. ; Christ et al. ; Davis ; Foster , references therein; Klowden ; Klowden ; Klowden and Blackmer ; Klowden and Lea ; and Vargo and Foster

Fig. 2

Patterns of antennal transcript abundance for select chemosensory gene families depicted during the first gonotrophic cycle of a female mosquito. The relative transcript abundance, as determined as the percent of the maximal average abundance over time (days) for each gene of the odorant receptor (Or, a, e), ionotropic receptor (Ir, b, f), and odorant binding protein (OBP, c, d, g, h) families, in the antennae of female Aedes aegypti are shown in box plots, with the whiskers denoting 5–95 percentile. Antennal transcript profiles were made from females with ad libitum access to sugar, and either no access to blood (a–d) or a complete blood meal at 5-day post-emergence (e–h). There are two evident motifs in transcript abundance, motif 1, as shown by the receptor families (a, b, e, f) and the majority of the expressed OBPs (c, g), and motif 2, as observed in the remaining 20% (d, h). Data presented here originate from Tallon et al. (2019) and Hill et al. (accepted). Note that data was not collected on days 2 and 4 for non-blood fed females, and as females were fed on day 5, no data is shown in days 1–4 for blood fed females