Size, sounds, and sex: interactions between body size and harmonic convergence signals determine mating success in Aedes aegypti

Background: Several new mosquito control strategies will involve the release of laboratory reared males which will be required to compete with wild males for mates. Currently, the determinants of male mating success remain unclear. The presence of convergence between male and female harmonic flight tone frequencies during a mating attempt have been found to increase male mating success in the yellow fever mosquito, Aedes aegypti. Size has also been implicated as a factor in male mating success. Here we investigated the relationships between body size, harmonic convergence signalling, and mating success. We predicted that harmonic convergence would be an important determinant of mating success and that large individuals would be more likely to converge. Methods: We used diet to manipulate male and female body size and then measured acoustic interactions during mating attempts between pairs of different body sizes. Additionally, we used playback experiments to measure the direct effect of size on signalling performance. Results: In live pair interactions, harmonic convergence was again found to be a significant predictor of copula formation. However, we additionally found interactions between harmonic convergence behaviour and body size. The probability that a given male successfully formed a copula was a consequence of his size, the size of the female encountered, and whether or not they converged. While convergence appears to be predictive of mating success regardless of size, the positive effect of convergence was modulated by size combinations. In playbacks, adult body size did not affect the probability of harmonic convergence responses. Conclusions: Both body size and harmonic convergence signalling were found to be determinants of male mating success. Our results suggest that in addition to measuring convergence ability of mass release lines that the size distribution of released males may need to be adjusted to complement the size distribution of females. We also found that diet amount alone cannot be used to increase male mating success or convergence probability. A clearer understanding of convergence behaviours, their relationship to mating success, and factors influencing convergence ability would provide the groundwork for improving the mating performance of laboratory reared lines

Alterations in mosquito behaviour by malaria parasites: potential impact on force of infection

BACKGROUND: A variety of studies have reported that malaria parasites alter the behaviour of mosquitoes. These behavioural alterations likely increase transmission because they reduce the risk of vector death during parasite development and increase biting after parasites become infectious. METHODS: A mathematical model is used to investigate the potential impact of these behavioural alterations on the lifetime number of infectious bites delivered. The model is used to explore the importance of assumptions about the magnitude and distribution of mortality as well as the importance of extrinsic incubation period and gonotrophic cycle length. Additionally, the model is applied to four datasets taken from actual transmission settings. RESULTS: The impact of behavioural changes on the relative number of lifetime bites is highly dependent on assumptions about the distribution of mortality over the mosquito-feeding cycle. Even using fairly conservative estimates of these parameters and field collected data, the model outputs suggest that altered feeding could easily cause a doubling in the force of infection. CONCLUSIONS: Infection-induced behavioural alterations have their greatest impact on the lifetime number of infectious bites in environments with high feeding-related adult mortality and many pre-infectious feeding cycles. Interventions that increase feeding-associated mortality are predicted to amplify the relative fitness benefits and hence enhance the strength of selection for behavioural alteration.This study was supported by the NIH-NIAID ICEMR award (#U19AI089676-01)

Oil palm expansion increases the vectorial capacity of dengue vectors in Malaysian Borneo

Changes in land-use and the associated shifts in environmental conditions can have large effects on the transmission and emergence of mosquito-borne disease. Mosquito-borne disease are particularly sensitive to these changes because mosquito growth, reproduction, survival and susceptibility to infection are all thermally sensitive traits, and land use change dramatically alters local microclimate. Predicting disease transmission under environmental change is increasingly critical for targeting mosquito-borne disease control and for identifying hotspots of disease emergence. Mechanistic models offer a powerful tool for improving these predictions. However, these approaches are limited by the quality and scale of temperature data and the thermal response curves that underlie predictions. Here, we used fine-scale temperature monitoring and a combination of empirical, laboratory and temperature-dependent estimates to estimate the vectorial capacity of Aedes albopictus mosquitoes across a tropical forest-oil palm plantation conversion gradient in Malaysian Borneo. We found that fine-scale differences in temperature between logged forest and oil palm plantation sites were not sufficient to produce differences in temperature-dependent demographic trait estimates using published thermal performance curves. However, when measured under field conditions a key parameter, adult abundance, differed significantly between land-use types, resulting in estimates of vectorial capacity that were 1.5 times higher in plantations than in forests. The prediction that oil palm plantations would support mosquito populations with higher vectorial capacity was robust to uncertainties in our adult survival estimates. These results provide a mechanistic basis for understanding the effects of forest conversion to agriculture on mosquito-borne disease risk, and a framework for interpreting emergent relationships between land-use and disease transmission. As the burden of Ae. albopictus-vectored diseases, such as dengue virus, increases globally and rising demand for palm oil products drives continued expansion of plantations, these findings have important implications for conservation, land management and public health policy at the global scale

The effect of resource limitation on the temperature-dependence of mosquito population fitness

Laboratory-derived temperature dependencies of life history traits are increasingly being used to make mechanistic predictions for how climatic warming will affect vector-borne disease dynamics, partially by affecting abundance dynamics of the vector population. These temperature-trait relationships are typically estimated from juvenile populations reared on optimal resource supply, even though natural populations of vectors are expected to experience variation in resource supply, including intermittent resource limitation. Using laboratory experiments on the mosquito Aedes aegypti, a principal arbovirus vector, combined with stage-structured population modelling, we show that low-resource supply in the juvenile life stages significantly depresses the vector’s maximal population growth rate across the entire temperature range (22–32°C) and causes it to peak at a lower temperature than at high-resource supply. This effect is primarily driven by an increase in juvenile mortality and development time, combined with a decrease in adult size with temperature at low-resource supply. Our study suggests that most projections of temperature-dependent vector abundance and disease transmission are likely to be biased because they are based on traits measured under optimal resource supply. Our results provide compelling evidence for future studies to consider resource supply when predicting the effects of climate and habitat change on vector-borne disease transmission, disease vectors and other arthropods

The effect of larval diet on adult survival, swarming activity and copulation success in male Aedes aegypti (Diptera: Culicidae)

Control of Aedes aegypti (L.) (Diptera: Culicidae) populations is vital for reducing the transmission of several pervasive human diseases. The success of new vector control technologies will be influenced by the fitness of laboratory-reared transgenic males. However, there has been relatively little published data on how rearing practices influence male fitness in Aedes mosquitoes. In the laboratory, the effect of larval food availability on adult male fitness was tested, using a range of different fitness measures. Larval food availability was demonstrated to be positively correlated with adult body size. Larger males survived longer and exhibited greater swarming activity. As a consequence, larger males may have more mating opportunities in the wild. However, we also found that within a swarm larger males did not have an increased likelihood of copulating with a female. The outcome of the mating competition experiments depended on the methodology used to mark the males. These results show that fitness assessment can vary depending on the measure analyzed, and the methodology used to determine it. Continued investigation into these fitness measures and methodologies, and critically, their utility for predicting male performance in the field, will increase the efficiency of vector control programs

SIT for African malaria vectors: Epilogue

As a result of increased support and the diligent application of new and conventional anti-malaria tools, significant reductions in malaria transmission are being accomplished. Historical and current evolutionary responses of vectors and parasites to malaria interventions demonstrate that it is unwise to assume that a limited suite of tools will remain effective indefinitely, thus efforts to develop new interventions should continue. This collection of manuscripts surveys the prospects and technical challenges for applying a novel tool, the sterile insect technique (SIT), against mosquitoes that transmit malaria. The method has been very successful against many agricultural pest insects in area-wide programs, but demonstrations against malaria vectors have not been sufficient to determine its potential relative to current alternatives, much of which will hinge ultimately upon cost. These manuscripts provide an overview of current efforts to develop SIT and identify key research issues that remain

Morphological Differentiation May Mediate Mate-Choice between Incipient Species of Anopheles gambiae s.s.

The M and S molecular forms of Anopheles gambiae s.s. have been considered incipient species for more than ten years, yet the mechanism underlying assortative mating of these incipient species has remained elusive. The discovery of the importance of harmonic convergence of wing beat frequency in mosquito mating and its relation to wing size have laid the foundation for exploring phenotypic divergence in wing size of wild populations of the two forms. In this study, wings from field collected mosquitoes were measured for wing length and wing width from two parts of the sympatric distribution, which differ with respect to the strength of assortative mating. In Mali, where assortative mating is strong, as evidenced by low rates of hybridization, mean wing lengths and wing widths were significantly larger than those from Guinea-Bissau. In addition, mean wing widths in Mali were significantly different between molecular forms. In Guinea-Bissau, assortative mating appears comparatively reduced and wing lengths and widths did not differ significantly between molecular forms. The data presented in this study support the hypothesis that wing beat frequency may mediate assortative mating in the incipient species of A. gambiae and represent the first documentation of a morphological difference between the M and S molecular forms

Atomic Force Microscopy Study of Nano-Physiological Response of Ladybird Beetles to Photostimuli

Background: Insects are of interest not only as the most numerous and diverse group of animals but also as highly efficient bio-machines varying greatly in size. They are the main human competitors for crop, can transmit various diseases, etc. However, little study of insects with modern nanotechnology tools has been done. Methodology/Principal Findings: Here we applied an atomic force microscopy (AFM) method to study stimulation of ladybird beetles with light. This method allows for measuring of the internal physiological responses of insects by recording surface oscillations in different parts of the insect at sub-nanometer amplitude level and sub-millisecond time. Specifically, we studied the sensitivity of ladybird beetles to light of different wavelengths. We demonstrated previously unknown blindness of ladybird beetles to emerald color (,500nm) light, while being able to see UV-blue and green light. Furthermore, we showed how one could study the speed of the beetle adaptation to repetitive flashing light and its relaxation back to the initial stage. Conclusions: The results show the potential of the method in studying insects. We see this research as a part of what might be a new emerging area of ‘‘nanophysiology’ ’ of insects

Spatial distribution and male mating success of Anopheles gambiae swarms

<p>Abstract</p> <p>Background</p> <p><it>Anopheles gambiae </it>mates in flight at particular mating sites over specific landmarks known as swarm markers. The swarms are composed of males; females typically approach a swarm, and leave <it>in copula</it>. This mating aggregation looks like a lek, but appears to lack the component of female choice. To investigate the possible mechanisms promoting the evolution of swarming in this mosquito species, we looked at the variation in mating success between swarms and discussed the factors that structure it in light of the three major lekking models, known as the female preference model, the hotspot model, and the hotshot model.</p> <p>Results</p> <p>We found substantial variation in swarm size and in mating success between swarms. A strong correlation between swarm size and mating success was observed, and consistent with the hotspot model of lek formation, the <it>per capita </it>mating success of individual males did not increase with swarm size. For the spatial distribution of swarms, our results revealed that some display sites were more attractive to both males and females and that females were more attracted to large swarms. While the swarm markers we recognize help us in localizing swarms, they did not account for the variation in swarm size or in the swarm mating success, suggesting that mosquitoes probably are attracted to these markers, but also perceive and respond to other aspects of the swarming site.</p> <p>Conclusions</p> <p>Characterizing the mating system of a species helps understand how this species has evolved and how selective pressures operate on male and female traits. The current study looked at male mating success of <it>An. gambiae </it>and discussed possible factors that account for its variation. We found that swarms of <it>An. gambiae </it>conform to the hotspot model of lek formation. But because swarms may lack the female choice component, we propose that the <it>An. gambiae </it>mating system is a lek-like system that incorporates characteristics pertaining to other mating systems such as scramble mating competition.</p