Neuromodulation and Differential Learning Across Mosquito Species

Abstract

Mosquitoes can learn to change their host-feeding behaviors, such as shifting activity times to avoid bednets or switching from biting animals to biting humans, leading to the transfer of zoonotic diseases. Dopamine is critical for insect learning, but its role in the antennal lobe remains unclear, and it is unknown whether different mosquito species learn the same odor cues. We assayed aversive olfactory learning and dopaminergic brain innervation in four mosquito species with different host preferences and report here that they differentially learn odors salient to their preferred host and innervation patterns vary across species. Using genetically-encoded GCaMP6s Aedes aegypti, we mapped odor-evoked antennal lobe activity and report that glomeruli tuned to “learnable” odors have significantly higher dopaminergic innervation. Changes in dopamine expression in the antennal lobes of diverse invertebrate species may be an evolutionary mechanism to adapt olfactory learning circuitry without changing brain structure and for mosquitoes an ability to adapt to other hosts when their preferred are no longer present.

Immunohistochemical Characterization of the Nervous System of Culex pipiens (Diptera, Culicidae)

“…The protein sequence of Rattus norvegicus targeted with anti-tyrosine-hydroxylase is approximately 50% homologous with Drosophila melanogaster and Culicinae mosquitoes. Nevertheless, and similar to previous reports, specifically labeled dopaminergic neurons were shown in both Drosophila melanogaster and Culex pipiens [ 40 , 101 , 102 , 103 ]. Since dopamine is involved in many behavioral patterns including learning, olfaction, and locomotion [ 98 , 100 , 104 , 105 , 106 , 107 ], which are reported to be altered in arbovirus-infected mosquitoes [ 23 , 30 , 31 , 32 ], the antibody used is advantageous for investigating neurotransmission and thus behavioral alterations among mosquito species and in pathogenetic studies.…”

“…Behavioral changes following a stimulus or a viral infection are likely to be based on the species-specific distribution of specialized neurons and the associated distribution of various neurotransmitters or neurotransmitter-related enzymes [ 36 , 40 , 42 ]. In the present study, the antibody for the neurotransmitter-related enzyme glutamine synthetase yielded a clear immunopositive signal in cell bodies of the nervous system in Drosophila melanogaster and Culex pipiens , similar to the immunoreactivity of earlier studies [ 36 , 67 ].…”

“…One factor contributing to the lack of knowledge represents limited information about the neuroanatomy and neurotransmission of many mosquito species, irrespective of extensive efforts to elucidate the structural and functional organization of their nervous systems [ 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 ]. In fact, most studies focus on Aedes and Anopheles species, although cross-species studies are highly important for understanding the underlying mechanisms of species-specific behavioral traits [ 40 , 42 ].…”

Odour-mediated host seeking and discrimination in mosquitoes : chemistry, neurobiology and behaviour

“…Both positive and negative feeding experiences of taking a blood meal from preferred or non-preferred hosts were demonstrated to modulate innate host preference, but the mechanism is unclear (Mwandawiro et al, 2000;Vantaux et al, 2014). Moreover, mosquitoes were demonstrated to learn olfactory cues in an associative manner (Tomberlin et al, 2006;Chilaka et al, 2012;Menda et al, 2013), but learning seems to be dependent on the identity or innate valence of an odour, as some, but not all, odours can be learned in classical conditioning experiments (Vinauger et al, 2014(Vinauger et al, , 2018Wolff et al, 2019).…”

Olfactory systems across mosquito species

“…Equally, mosquitoes present us with unique opportunities to study unexplored processes that regulate olfactory sensitivity, rapid evolution of olfactory receptors and olfactory signals (Neafsey et al 2015), relations between olfaction and speciation (Coetzee et al 2013;Bradshaw et al 2018) and the effect of climate change, urbanisation and invasions on sensory systems (Balkew et al 2020;Rose et al 2020). We may wish to look beyond the olfactory receptors and study the processing of signals in the mosquito brain, which opens up a whole new set of questions concerning multisensory integrations and feedbacks (Vinauger et al 2019), the importance of trade-offs between brain areas devoted to different sensory modalities (Keesey et al 2019) and the effects of learning (Lutz et al 2017;Vinauger et al 2018;Wolff et al 2019).…”