Over the past two decades, control efforts have halved malaria cases globally, yet burdens remain high in much of Africa and elimination has not been achieved even where extreme reductions have occurred over many years, such as in South Africa 1,2 . Studies seeking to understand the paradoxical persistence of malaria in areas where surface water is absent for 3-8 months of the year, suggested that certain Anopheles mosquitoes employ long-distance migration 3 . Here, we confirmed this hypothesis by aerial sampling of mosquitoes 40-290 m above ground, providing the first evidence of windborne migration of African malaria vectors, and consequently the pathogens they transmit. Ten species, including the primary malaria vector Anopheles coluzzii, were identified among 235 anophelines captured during 617 nocturnal aerial collections in the Sahel of Mali. Importantly, females accounted for >80% of all mosquitoes collected. Of these, 90% had taken a blood meal before their migration, implying that pathogens will be transported long distances by migrating females. The likelihood of capturing Anopheles species increased with altitude and during the wet seasons, but variation between years and localities was minimal. Simulated trajectories of mosquito flights indicated mean nightly displacements of up to 300 km for 9-hour flight durations. Annually, the estimated numbers of mosquitoes at altitude crossing a 100-km line perpendicular to the winds included 81,000 An. gambiae s.s., 6 million An. coluzzii, and 44 million An. squamosus. These results provide compelling evidence that millions of previously blood-fed, malaria vectors frequently migrate over hundreds of kilometers, and thus almost certainly spread malaria over such distances. Malaria elimination success may, therefore, depend on whether sources of migrant vectors can be identified and
The African malaria mosquito, Anopheles gambiae, inhabits diverse environments including dry savannas, where surface waters required for larval development are absent for 4–8 months per year. Under such conditions, An. gambiae virtually disappears. Whether populations survive the long dry season by aestivation (a dormant state promoting extended longevity during the summer) or are reestablished by migrants from distant locations where larval sites persist has remained an enigma for over 60 years. Resolving this question is important, because fragile dry season populations may be more susceptible to control. Here, we show unequivocally that An. gambiae aestivates based on a demographic study and a mark release–recapture experiment spanning the period from the end of one wet season to the beginning of the next. During the dry season, An. gambiae was barely detectable in Sahelian villages of Mali. Five days after the first rain, before a new generation of adults could be produced, mosquito abundance surged 10-fold, implying that most mosquitoes were concealed locally until the rain. Four days after the first rain, a marked female An. gambiae s.s. was recaptured. Initially captured, marked, and released at the end of the previous wet season, she has survived the 7-month-long dry season. These results provide evidence that An. gambiae persists throughout the dry season by aestivation and open new questions for mosquito and parasite research. Improved malaria control by targeting aestivating mosquitoes using existing or novel strategies may be possible.
BackgroundAnopheles gambiae 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 in copula. 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.ResultsWe 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 per capita 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.ConclusionsCharacterizing 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 An. gambiae and discussed possible factors that account for its variation. We found that swarms of An. gambiae conform to the hotspot model of lek formation. But because swarms may lack the female choice component, we propose that the An. gambiae mating system is a lek-like system that incorporates characteristics pertaining to other mating systems such as scramble mating competition.
BackgroundPersistence of African anophelines throughout the long dry season (4-8 months) when no surface waters are available remains one of the enduring mysteries of medical entomology. Recent studies demonstrated that aestivation (summer diapause) is one mechanism that allows the African malaria mosquito, Anopheles gambiae, to persist in the Sahel. However, migration from distant localities - where reproduction continues year-round - might also be involved.MethodsTo assess the contribution of aestivating adults to the buildup of populations in the subsequent wet season, two villages subjected to weekly pyrethrum sprays throughout the dry season were compared with two nearby villages, which were only monitored. If aestivating adults are the main source of the subsequent wet-season population, then the subsequent wet-season density in the treated villages will be lower than in the control villages. Moreover, since virtually only M-form An. gambiae are found during the dry season, the reduction should be specific to the M form, whereas no such difference is predicted for S-form An. gambiae or Anopheles arabiensis. On the other hand, if migrants arriving with the first rain are the main source, no differences between treated and control villages are expected across all members of the An. gambiae complex.ResultsThe wet-season density of the M form in treated villages was 30% lower than that in the control (P < 10-4, permutation test), whereas no significant differences were detected in the S form or An. arabiensis.ConclusionsThese results support the hypothesis that the M form persist in the arid Sahel primarily by aestivation, whereas the S form and An. arabiensis rely on migration from distant locations. Implications for malaria control are discussed.
The African malaria mosquito, Anopheles gambiae, is widespread south of the Sahara including in dry savannahs and semi-arid environments where no surface water exists for several months a year. Adults of the M form of An. gambiae persist through the long dry season, when no surface waters are available, by increasing their maximal survival from 4 weeks to 7 months. Dry season diapause (aestivation) presumably underlies this extended survival. Diapause in adult insects is intrinsically linked to depressed reproduction. To determine if reproduction of the Sahelian M form is depressed during the dry season, we assessed seasonal changes in oviposition, egg batch size, and egg development, as well as insemination rate and blood feeding in wild caught mosquitoes. Results from xeric Sahelian and riparian populations were compared. Oviposition response in the Sahelian M form dropped from 70% during the wet season to 20% during the dry season while the mean egg batch size among those that laid eggs fell from 173 to 101. Correspondingly, the fraction of females that exhibited gonotrophic dissociation increased over the dry season from 5% to 45%, while a similar fraction of the population retained developed eggs despite having access to water. This depression in reproduction the Sahelian M form was not caused by a reduced insemination rate. Seasonal variation in these reproductive parameters of the riparian M form population was less extreme and the duration of reproductive depression was shorter. Blood feeding responses did not change with the season in either population. Depressed reproduction during the dry season in the Sahelian M form of An. gambiae provides additional evidence for aestivation and illuminates the physiological processes involved. The differences between the Sahelian and riparian population suggest an adaptive cline in aestivation phenotypes between populations only 130 km apart.
SUMMARYMalaria in Africa is vectored primarily by the Anopheles gambiae complex. Although the mechanisms of population persistence during the dry season are not yet known, targeting dry season mosquitoes could provide opportunities for vector control. In the Sahel, it appears likely that M-form A. gambiae survive by aestivation (entering a dormant state). To assess the role of ecophysiological changes associated with dry season survival, we measured body size, flight activity and metabolic rate of wildcaught mosquitoes throughout 1year in a Sahelian locality, far from permanent water sources, and at a riparian location adjacent to the Niger River. We found significant seasonal variation in body size at both the Sahelian and riparian sites, although the magnitude of the variation was greater in the Sahel. For flight activity, significant seasonality was only observed in the Sahel, with increased flight activity in the wet season when compared with that just prior to and throughout the dry season. Whole-organism metabolic rate was affected by numerous biotic and abiotic factors, and a significant seasonal component was found at both locations. However, assay temperature accounted completely for seasonality at the riparian location, while significant seasonal variation remained after accounting for all measured variables in the Sahel. Interestingly, we did not find that mean metabolic rate was lowest during the dry season at either location, contrary to our expectation that mosquitoes would conserve energy and increase longevity by reducing metabolism during this time. These results indicate that mosquitoes may use mechanisms besides reduced metabolic rate to enable survival during the Sahelian dry season. Supplementary material available online at
Mosquito swarms are poorly understood mating aggregations. In the malaria vector Anopheles gambiae Giles, they are known to depend on environmental conditions, such as the presence of a marker on the ground, and they may be highly relevant to reproductive isolation. We present quantitative measurements of individual An. gambiae positions within swarms from Donéguébougou, Mali, estimated by stereoscopic video image analysis. Results indicate that swarms in this species are approximately spherical, with an unexpectedly high density of individuals close to the swarm centroid. This high density may be the result of individual males maximizing their probability of encountering a female or a product of mosquito orientation through cues within the swarm. Our analysis also suggests a difference in swarm organization between putative incipient species of An. gambiae with increasing numbers of males. This may be related to a difference in marker use between these groups, supporting the hypothesis that swarming behavior is a mechanism of mate recognition and ultimately reproductive isolation. KeywordsAnopheles gambiae; swarm; mate recognition; three-dimensional localization; stereoscopic image analysis Mosquito swarms have long been observed and described, but with few exceptions (such as Gibson 1985), their physical organization and dynamics remain poorly understood, especially in the field. In this paper, we address two fundamental issues as they relate to swarms of the malaria vector Anopheles gambiae Giles. The first is how swarms of males are organized in this species. The second is what role this organization might play in mate choice and reproductive isolation within the An. gambiae species complex.Part of the reason little is known about mosquito swarms is that they are generally difficult to study in a natural setting. Locating the swarms can be difficult for many species (Service 1993), and even once found, it is difficult to gather quantitative measurements (although not impossible; see Yuval and Bouskila 1993). Previous studies on insect swarming generally used image acquisition and processing techniques to examine swarms (Okubo et al. 1981, Riley 1993. Stereoscopic image analysis in particular has been used to study mosquito swarms, resulting in some sophisticated statistical methods for localizing individuals (Ikawa and Okabe 1997). However, these approaches have yielded limited biological insight into the organization 2Corresponding author, e-mail: E-mail: manoukisn@niaid.nih.gov. Anopheles gambiae swarms are known to be composed almost entirely of males (Diabaté et al. 2006), and are often, although not always, found over "swarming markers" (Marchand 1984, Charlwood et al. 2002. As in other dipterans, they are thought to be mating aggregations (Downes 1969, Sullivan 1981. They probably fit the strict definition of a lek (an area where males congregate to secure mates), especially because they represent non-resource-based aggregations. There may be competition for more advantageous positions within t...
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