Highlights d Key Drosophila thermosensors detect heating and cooling, rather than hot and cold d Ionotropic Receptors (IRs) mediate cooling detection d IRs specify both the morphogenesis and thermosensitivity of sensory endings d Thermoregulation requires context-dependent interpretation of phasic sensory inputs

Mosquitoes transmit pathogens that kill >700,000 people annually. These insects use body heat to locate and feed on warm-blooded hosts, but the molecular basis of such behavior is unknown. Here, we identify ionotropic receptor IR21a, a receptor conserved throughout insects, as a key mediator of heat seeking in the malaria vector Anopheles gambiae. Although Ir21a mediates heat avoidance in Drosophila, we find it drives heat seeking and heat-stimulated blood feeding in Anopheles. At a cellular level, Ir21a is essential for the detection of cooling, suggesting that during evolution mosquito heat seeking relied on cooling-mediated repulsion. Our data indicate that the evolution of blood feeding in Anopheles involves repurposing an ancestral thermoreceptor from non–blood-feeding Diptera.

Accurate perception of taste information is crucial for animal survival. In adult Drosophila, gustatory receptor neurons (GRNs) perceive chemical stimuli of one specific gustatory modality associated with a stereotyped behavioural response, such as aversion or attraction. We show that GRNs of Drosophila larvae employ a surprisingly different mode of gustatory information coding. Using a novel method for calcium imaging in the larval gustatory system, we identify a multimodal GRN that responds to chemicals of different taste modalities with opposing valence, such as sweet sucrose and bitter denatonium, reliant on different sensory receptors. This multimodal neuron is essential for bitter compound avoidance, and its artificial activation is sufficient to mediate aversion. However, the neuron is also essential for the integration of taste blends. Our findings support a model for taste coding in larvae, in which distinct receptor proteins mediate different responses within the same, multimodal GRN.

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The ionotropic receptors (IRs) are a branch of the ionotropic glutamate receptor family and serve as important mediators of sensory transduction in invertebrates. Recent work shows that, though initially studied as olfactory receptors, the IRs also mediate the detection of taste, temperature, and humidity. Here, we summarize recent insights into IR evolution and its potential ecological significance as well as recent advances in our understanding of how IRs contribute to diverse sensory modalities.