Abstract
BackgroundBehavioural shifts in the canonical location and timing of biting have been reported in natural populations of anopheline malaria vectors following the implementation of insecticide-based indoor vector control interventions. These modifications increase the likelihood of human-vector contact and allow mosquitoes to avoid insecticides, both conditions being favourable to residual transmission of the malarial parasites. The biting behaviour of mosquitoes follows rhythms that are under the control of biological clocks and environmental conditions, modulated by physiological states. In this work we explore modifications of spontaneous locomotor activity expressed by mosquitoes in different physiological states to highlight phenotypic variability associated to circadian control that may contribute to explain residual transmission in the field.MethodsThe F10 generation progeny of field-collected Anopheles coluzzii from southwestern Burkina Faso was tested using an automated recording apparatus (Locomotor Activity Monitor, TriKinetics Inc.) under LD 12:12 or DD light regimens in laboratory-controlled conditions. Activity recordings of each test were carried out for a week with 6-day-old females belonging to four experimental treatments, representing factorial combinations of two physiological variables: insemination status (virgin vs inseminated) and gonotrophic status (glucose fed vs blood fed). Chronobiological features of rhythmicity in locomotor activity were explored using periodograms, diversity indices, and generalized linear mixed modelling.ResultsThe average strength of activity, onset of activity, and acrophase were modulated by both nutritional and insemination status as well as by the light regimen. Inseminated females showed a significant excess of arrhythmic activity under DD. When rhythmicity was observed in DD, females displayed sustained activity also during the subjective day.ConclusionsInsemination and gonotrophic status influence the underlying light and circadian control of chronobiological features of locomotor activity. Overrepresentation of arrhythmic chronotypes as well as the sustained activity of inseminated females during the subjective day under DD conditions suggests potential activity of natural populations of A. coluzzii during daytime under dim conditions, with implications for residual transmission of malarial parasites.Graphical abstract
Highlights
Behavioural shifts in the canonical location and timing of biting have been reported in natural populations of anopheline malaria vectors following the implementation of insecticide-based indoor vector control interventions
We worked on the tenth generation of mosquitoes after their introduction in our insectary. This was the time that had elapsed since the collection from the field and the establishment of the working colony, which was necessary to select for insecticide-susceptible A. coluzzii only, to allow females to adapt to our insectary routines, to obtain successful and optimal blood-feeding during the day, to optimise our feeding protocol during the recording to increase females survival in the tubes, and to reach the number of offspring needed to create our working groups simultaneously
This study aimed at investigating how fundamental physiological changes induced by mating and blood feeding interact in modulating the spontaneous locomotor activity of females of the malaria mosquito A. coluzzii
Summary
Behavioural shifts in the canonical location and timing of biting have been reported in natural populations of anopheline malaria vectors following the implementation of insecticide-based indoor vector control interventions These modifications increase the likelihood of human-vector contact and allow mosquitoes to avoid insecticides, both conditions being favourable to residual transmission of the malarial parasites. After complete maturation of the oocytes the female is ready to engage in her quest for a suitable water collection where to lay eggs After oviposition, another gonotrophic cycle (i.e. the cyclical repetition of the sequence of the physiologically controlled blood-feeding, resting, and oviposition behaviours) is engaged, and this is repeated throughout the female’s lifetime. Embedded within the infradian rhythmicity of the gonotrophic cycle, which follows a sequence of gated physiological changes, each of these behaviours is usually associated with circadian periodicities modulated by diel changes in peripheral receptors’ sensitivity to key stimuli [6, 23, 24] or changes in behavioural responsiveness [25,26,27], but above all the overt expression of behaviours is regulated by the circadian rhythmicity of general activity under the control of molecular clocks [28, 29]
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