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Georgiades, M.

Publications and source records attributed to Georgiades, M..

6 recordsLinked to original sources

Distortion rules: audibility creation in the mosquito ear

Hearing begins when ears convert sound into neuronal excitation. The hearing organs of male Anopheles mosquitoes rank amongst the most sensitive ears evolved. Males use them to detect faint female flight tones within noisy mating swarms, but female flight tones largely lie above the males hearing range. We report a mechanism by which inaudible higher-frequency primary tones become audible through intrinsically generated, lower-frequency distortion tones. Distortion-evoked responses show [~]10-times greater sensitivity and 45% higher temporal precision than those of same-frequency primary tones. Moreover, self-sustained oscillations of the males ear dramatically reshape auditory frequency tuning and neuronal recruitment. By one mechanism, mosquito ears thus create audible signals and isolate these from the most salient frequencies of background noise. In audiology, distortions are used for diagnostics; their biological relevance, however, is unknown. Our results suggest that distortions are not mere by-products of the auditory process, but integral to its signaling logic.

neuroscience↗

Using a female-specific isoform of doublesex to explore male-specific hearing in mosquitoes

Animal reproduction relies on elaborate divisions of labour and multiple dimorphisms between the sexes. Primary dimorphisms affect core elements of reproduction, secondary dimorphisms affect more indirect traits, including complex behaviours. In disease-transmitting mosquitoes, males locate females acoustically prior to copulation (phonotaxis). No comparable acoustic behaviour is known for females. As a result, the males ears - and hearing performance - have evolved to become substantially more complex. Sex-specific hearing in mosquitoes is in part controlled by the doublesex (dsx) gene. Intriguingly, dsx forms a linker between primary and secondary dimorphisms: spermatogenesis and ear morphogenesis share considerable molecular overlap and both depend on dsx expression patterns. We have combined transcriptomics with functional-anatomical analyses to dissect dsx-dependent hearing in the malaria mosquito Anopheles gambiae. By cross-linking our auditory findings to the genetic bases of spermatogenesis we advance the molecular understanding of sex-specific hearing mechanisms in insects, highlighting the special roles of ciliary factors therein. HighlightsO_LIDisruption of the female-specific exon of the doublesex gene alters hearing in female Anopheles gambiae mosquitoes C_LIO_LIFemale mutant ears are anatomically and functionally distinct from both wild-type male and female; they show a substantial, but incomplete, masculinisation C_LIO_LIContrary to males, and similarly to females, the flagella of female mutants do not exhibit Self-Sustained Oscillations (SSOs) C_LIO_LITranscriptomic comparisons of ears uncovered molecular bases of auditory maleness, these were closely linked to molecular machinery of ciliary function C_LIO_LIComparisons with existing transcriptome from male testes revealed a substantial overlap between male ear and testicular ciliary motility machineries C_LI

neuroscience↗

The GABAA receptor RDL modulates the auditory sensitivity of malaria mosquitoes.

Malaria mosquitoes mate in crowded, and noisy, swarms. A vital stage of their precopulatory behaviour involves detecting the faint flight tone of a mating partner amidst the noise from hundreds of other mosquitoes. This exquisite sensory performance is enabled by a complex auditory system with remarkable features. One such feature is their vast efferent control system, which provides the mosquito ear with the required plasticity to adapt to various external and internal changes. In this paper, we study the auditory role of GABA, one of the main efferent signalling molecules in the mosquito ear, and its interactions with octopamine, another neurotransmitter of the efferent network. We show that GABA is released in the malaria mosquito auditory nerve and that GABA receptors are expressed in the ear, including the GABAA receptor Resistance to Dieldrin (RDL), a target for the evolution of insecticide resistance. Using picrotoxin to antagonize RDL receptors, we discovered multiple auditory effects of GABA at the mechanical and electrical level. At the mechanical level, blocking RDL promotes the erection of antennal fibrillae and the cessation of flagellar self-sustained oscillations. These effects are not observed in knockouts of the octopamine receptor AgOct{beta}2, suggesting that RDL auditory mechanical effects are mediated through octopamine release in the mosquito ear. Electrically, picrotoxin injection increases the spontaneous firing of auditory neurons and direct current (DC) responses of the nerve to mechanical stimulation both in wildtype and AgOct{beta}2 mutants, indicating that RDL may also modulate auditory sensitivity via octopamine-independent pathways. In summary, our experiments uncover distinct auditory roles of GABA, as well as synergistic roles with octopamine. The data show a fundamental role of RDL in controlling the auditory function of malaria mosquitoes and implicate RDL signalling in mating of natural malaria mosquito populations.

neuroscience↗

A novel beta-adrenergic like octopamine receptor modulates the audition of malaria mosquitoes and serves as insecticide target

Hearing is an essential sense in the life cycle of malaria mosquitoes. Within large swarms formed transiently at dusk, mosquitoes acoustically recognize their mating partners by their wingbeats. Indeed, malaria mosquitoes only respond to the flight tones of mating partners during swarm time. This phenomenon implies a sophisticated context- and time-dependent modulation of mosquito audition, the mechanisms of which are still largely unknown. Using transcriptomics, we identify a complex network of candidate neuromodulators regulating mosquito hearing. Among them, octopamine stands out as regulator of the auditory performance during swarm time. To explore octopamines roles in mosquito hearing, we carried out an in-depth analysis of octopamine-mediated effects on auditory function. We found that octopamine affects the properties of the mosquito ear on multiple levels: it modulates the tuning and stiffness of the flagellar sound receiver and it controls the erection of antennal fibrillae in males. We found that two different receptors are driving octopamines auditory roles, including a novel beta octopamine receptor. We also demonstrate that the octopaminergic auditory control system can be targeted by insecticides. Our findings identify octopamine signalling as a key component of hearing and mating partner detection in malaria mosquitoes, and as a potential novel target for mosquito control.

neuroscience↗

Flight-tone mediated circadian control of audibility in mating swarms of Anopheles mosquitoes

Mating swarms of malaria mosquitoes form every day at sunset throughout the tropical world, they typically last less than 30 minutes. Activity patterns must thus be highly synchronized between the sexes. Moreover, males must be able to identify the few sporadically entering females by detecting the females faint flight tones. We here show that the Anopheles circadian clock ensures a tight synchrony of male and female activity and -importantly - also retunes the males acoustic detection system: by lifting their own flight tones at dusk, males actively enhance the audibility of females. The reported phenomenon of harmonic convergence is a random by-product of the mosquitoes flight tone variance. Intriguingly, flight tones of individual mosquitoes occupy narrow -partly non-overlapping-frequency ranges, suggesting that the audibility of individual females varies across males. One Sentence SummaryMale mosquitoes sharpen their hearing at sunset.

neuroscience↗

Assessing the acoustic behaviour of Anopheles gambiae s.l. dsxF mutants: Implications for Vector Control

BackgroundThe release of genetically modified mosquitoes which use gene-drive mechanisms to suppress reproduction in natural populations of Anopheles mosquitoes is one of the scientifically most promising methods for malaria transmission control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. Mutations which reduce an individuals reproductive success are likely to create strong selective pressures to evolve resistance. It is thus crucial that the targeted population collapses as rapidly and as completely as possible to reduce the available time for the emergence of drive-resistant mutations. At a behavioural level, this means that the gene-drive carrying mutants should be at least as (and ideally more) sexually attractive than the wildtype population they compete against. A key element in the copulatory negotiations of Anopheles mosquitoes is their acoustic courtship. We therefore analysed sound emissions and acoustic preference in a doublesex mutant previously used to successfully collapse caged colonies of Anopheles gambiae s.l.. MethodsThe flight tones produced by the beating of their wings form the signals for acoustic mating communication in Anopheles species. We assessed the acoustic impact of the disruption of a female-specific isoform of the doublesex gene (dsxF) on the wing beat frequency (WBF; measured as flight tone) of both males (XY) and females (XX) in homozygous dsxF- mutants (dsxF-/-), heterozygous dsxF- carriers (dsxF+/-) and G3 wildtype dsxF+ controls (dsxF+/+). To exclude non-genetic influences, we controlled for temperature and measured wing lengths for all experimental animals. We used a phonotaxis assay to test the acoustic preferences of mutant and control mosquitoes. ResultsA previous study demonstrated an altered phenotype only for females homozygous for the disrupted dsx allele (dsxF-/-), who appear intersex. No phenotypic changes were observed for heterozygous carriers or males, suggesting that the female-specific dsxF allele is haplosufficient. We here identify significant, dose-dependent increases in the flight tones of both dsxF-/- and dsxF+/- females when compared to dsxF+/+ control females. Flight tone frequencies in all three female genotypes remained significantly lower than in males, however. When tested experimentally, males showed stronger phonotactic responses to the flight tones of control dsxF+/+ females. While flight tones from dsxF+/- and dsxF-/- females also elicited positive phonotactic behaviour in males, this was significantly reduced compared to responses to control tones. We found no evidence of phonotactic behaviour in any female genotype tested. None of the male genotypes displayed any deviations from the control condition. ConclusionsA key prerequisite for copulation in anopheline mosquitoes is the phonotactic attraction of males towards female flight tones within large - spatially and acoustically crowded - mating swarms. Reductions in acoustic attractiveness of released mutant lines, as reported here for heterozygous dsxF+/- females, reduce the lines mating efficiency, and could consequently reduce the efficacy of the associated population control effort. Assessments of caged populations may not successfully reproduce the challenges posed by natural mating scenarios. We propose to amend existing testing protocols in order to more faithfully reflect the competitive conditions between a mutant line and the wildtype population it is meant to interact with. This should also include novel tests of acoustic fitness. In line with previous studies, our findings confirm that disruption of the female-specific isoform dsxF has no effect on males; for some phenotypic traits, such as female flight tones, however, the effects of dsxF appear to be dose-dependent rather than haplosufficient.

animal behavior and cognition↗