T Lehmann

National Institute of Allergy and Infectious Diseases, Maryland, United States

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Publications (88)293.02 Total impact

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    ABSTRACT: During the long Sahelian dry season, mosquito vectors of malaria are expected to perish when no larval sites are available; yet, days after the first rains, mosquitoes reappear in large numbers. How these vectors persist over the 3-6-month long dry season has not been resolved, despite extensive research for over a century. Hypotheses for vector persistence include dry-season diapause (aestivation) and long-distance migration (LDM); both are facets of vector biology that have been highly controversial owing to lack of concrete evidence. Here we show that certain species persist by a form of aestivation, while others engage in LDM. Using time-series analyses, the seasonal cycles of Anopheles coluzzii, Anopheles gambiae sensu stricto (s.s.), and Anopheles arabiensis were estimated, and their effects were found to be significant, stable and highly species-specific. Contrary to all expectations, the most complex dynamics occurred during the dry season, when the density of A. coluzzii fluctuated markedly, peaking when migration would seem highly unlikely, whereas A. gambiae s.s. was undetected. The population growth of A. coluzzii followed the first rains closely, consistent with aestivation, whereas the growth phase of both A. gambiae s.s. and A. arabiensis lagged by two months. Such a delay is incompatible with local persistence, but fits LDM. Surviving the long dry season in situ allows A. coluzzii to predominate and form the primary force of malaria transmission. Our results reveal profound ecological divergence between A. coluzzii and A. gambiae s.s., whose standing as distinct species has been challenged, and suggest that climate is one of the selective pressures that led to their speciation. Incorporating vector dormancy and LDM is key to predicting shifts in the range of malaria due to global climate change, and to the elimination of malaria from Africa.
    Nature 11/2014; 516(7531). DOI:10.1038/nature13987 · 42.35 Impact Factor
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    R Faiman, DL Huestis, T Lehmann
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    ABSTRACT: Adult mosquitoes feed on plant sugars or aphid honeydew for their energy requirements. Females obtain blood as a source of protein for egg maturation mostly. Anopheles gambiae search for sugars prior to foraging for blood, and continue to sugar-feed during and after egg development. In Drosophila sp., it was recently shown that dietary restriction (DR), manifested as a modest reduction in sugar and/or protein intake, resulted in relative prolonged lifespan. This was hypothesized to be a conserved evolutionary process for selection of individuals capable of surviving and reproducing after prolonged unfavorable conditions. Nutritional Geometry theory claims that the Carbohydrate : Protein ratio influences longevity and reproduction, more than the total amount of carbohydrates, calories and/or proteins alone. Here, we explore the effect of carbohydrate and protein availability on An. coluzzii lifespan as part of the effort to simulate dormancy under laboratory conditions. Environmental factors tested include temperature, relative humidity (RH), and photoperiod in addition to dietary restriction and composition. This experiment is designed to identify the combination of conditions that promote the greatest extension of longevity as a proxy of dormancy. Preliminary results are presented. Methods • Pilot study: Choosing the right sugar. • Females (mated) tested in groups of 30 in half-gallon cages (n=20). • Ten cages tested under short photoperiod, cooler conditions (22°C, 85% RH). • Ten cages tested under long photoperiod, warmer conditions (27°C , 85% RH). • Within each photoperiod/temperature group, five cages were maintained under lower RH conditions (±50%). • Nutritional treatments: • severe/moderate/no sugar restriction. • severe/moderate/no blood restriction. • Sugar was given in the form of a 25% organic honey solution, in removable glass flasks. • Bovine blood was offered through hog-gut membrane on a water-heated feeder at 38°C for 30 minutes. • Oviposition cups were provided to high RH treatments only. Eggs were tallied. • Female mortality counts made daily. Dead females will be dissected for insemination rate, retained eggs evaluation and feeding rate . 85% RH 55% RH 85% RH 55% RH Environmental conditions setup Short day 27°C 22°C Results 3 days / week 1 day / week Every week Every other week None Carbohydrate restriction (C) (Honey, 25%) Protein restriction (P) (blood-meals) 7 days / week Nutritional conditions setup • Sugars pilot study: no significant differences found between sucrose, glucose, fructose and honey in mosquitoes survival. • Honey chosen for experiment for its highest resemblance to floral nectar (Foster & Takken, 2004) • Only treatments relevant to either field-measured or hypothesized conditions are tested (5 of 9 C:P combinations). • Study in progress and currently into its fourth week. • To date: treatments with low temperature, and moderate sugar and blood restriction hold the highest survival rates (see graphs).
    ASTMH 63rd Annual Meeting, New Orleans, LA; 11/2014
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    ABSTRACT: Background Increased understanding of the dry-season survival mechanisms of Anopheles gambiae in semi-arid regions could benefit vector control efforts by identifying weak links in the transmission cycle of malaria. In this study, we examined the effect of photoperiod and relative humidity on morphologic and chemical traits known to control water loss in mosquitoes. Methods Anopheles gambiae body size (indexed by wing length), mesothoracic spiracle size, and cuticular hydrocarbon composition (both standardized by body size) were examined in mosquitoes raised from eggs exposed to short photoperiod and low relative humidity, simulating the dry season, or long photoperiod and high relative humidity, simulating the wet-season. Results Mosquitoes exposed to short photoperiod exhibited larger body size and larger mesothoracic spiracle length than mosquitoes exposed to long photoperiod. Mosquitoes exposed to short photoperiod and low relative humidity exhibited greater total cuticular hydrocarbon amount than mosquitoes exposed to long photoperiod and high relative humidity. In addition, total cuticular hydrocarbon amount increased with age and was higher in mated females. Mean n-alkane retention time (a measure of cuticular hydrocarbon chain length) was lower in mosquitoes exposed to short photoperiod and low relative humidity, and increased with age. Individual cuticular hydrocarbon peaks were examined, and several cuticular hydrocarbons were identified as potential biomarkers of dry- and wet-season conditions, age, and insemination status. Conclusions Results from this study indicate that morphological and chemical changes underlie aestivation of Anopheles gambiae and may serve as biomarkers of aestivation.
    Parasites & Vectors 06/2014; 7(1):294. DOI:10.1186/1756-3305-7-294 · 3.25 Impact Factor
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    Diana L Huestis, Tovi Lehmann
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    ABSTRACT: The dry-season biology of malaria vectors is poorly understood, especially in arid environments when no surface waters are available for several months, such as during the dry season in the Sahel. Here we reappraise results on the dry-season physiology of members of the Anopheles gambiae s.l. complex in the broad context of dormancy in insects and especially in mosquitoes. We examine evidence on seasonal changes in reproduction, metabolism, stress tolerance, nutrition, molecular regulation, and environmental conditions and determine if the current results are compatible with dry-season diapause (aestivation) as the primary strategy for persistence throughout the dry season in the Sahel. In the process, we point out critical gaps in our knowledge that future studies can fill. We find compelling evidence that members of the An. gambiae s.l. complex undergo a form of aestivation during the Sahelian dry season by shifting energetic resources away from reproduction and towards increased longevity. Considering the differences between winter at temperate latitudes, which entails immobility of the insect and hence reliance on physiological solutions, as opposed to the Sahelian dry season, which restricts reproduction exclusively, we propose that behavioral changes play an important role in complementing physiological changes in this strategy.
    Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 06/2014; DOI:10.1016/j.meegid.2014.05.027 · 3.26 Impact Factor
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    ABSTRACT: The African malaria mosquito, Anopheles gambiae, needs surface water in order to lay their eggs. In many parts of Africa, there are dry periods varying from days to months in length when suitable larval sites are not available and female mosquitoes experience oviposition-site deprivation (OSD). Previous studies have shown that egg-laying and egg-hatching rates were reduced due to OSD. Here, we assessed its effect on longevity and bloodfeeding rate of Anopheles gambiae. We predicted that OSD will increase mosquito longevity and the aptitude of mosquitoes to take additional blood meals; importantly, these changes will increase its vectorial capacity. To measure the effect of OSD, four treatments were utilized: two oviposition-deprived groups, one of which was bloodfed once (OBOD) and one that was bloodfed weekly (MBOD); a non-oviposition-deprived, a weekly bloodfed control group (MBC); and a blood-deprived age-control group (BD). Mortality was assessed daily and bloodfeeding rate was measured at weekly intervals. Under OSD, survival of female A. gambiae was reduced by 10-20%, reflecting reduction of the MBOD and OBOD groups from the MBC group, respectively. Likewise, bloodfeeding response during three weeks of OSD was reduced but the reduction varied as a function of time from the last blood meal. These results indicate that OSD is expected to reduce A. gambiae vectorial capacity and that OSD alone does not act as cue used by female mosquitoes to switch into a dormant state of extended survivorship with reproductive quiescence.
    Parasites & Vectors 04/2014; 7(1):163. DOI:10.1186/1756-3305-7-163 · 3.25 Impact Factor
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    ABSTRACT: Changes in spatial distribution of mosquitoes over time in a Sahelian village were studied to understand the sources of the mosquitoes during the dry season when no larval sites are found. At that time, the sources of Anopheles gambiae Giles may be local shelters used by aestivating mosquitoes or migrants from distant populations. The mosquito distribution was more aggregated during the dry season, when few houses had densities 7- to 24-fold higher than expected. The high-density houses during the dry season differed from those of the wet season. Most high-density houses during the dry season changed between years, yet their vicinity was rather stable. Scan statistics confirmed the presence of one or two adjacent hotspots in the dry season, usually found on one edge of the village. These hotspots shifted between the early and late dry season. During the wet season, the hotspots were relatively stable near the main larval site. The locations of the hotspots in the wet season and early and late dry season were similar between years. Season-specific, stable, and focal hotspots are inconsistent with the predictions based on the arrival of migrants from distant localities during the dry season, but are consistent with the predictions based on local shelters used by aestivating mosquitoes. Targeting hotspots in Sahelian villages for vector control may not be effective because the degree of aggregation is moderate, the hotspots are not easily predicted, and they are not the sources of the population. However, targeting the dry-season shelters may be highly cost-effective, once they can be identified and predicted.
    Journal of Medical Entomology 01/2014; 51(1):27-38. DOI:10.1603/ME13094 · 1.82 Impact Factor
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    ABSTRACT: The molecular form composition of Anopheles gambiae Giles s.s. (Diptera: Culicidae) mating swarms and the associated mating pairs (copulae) were investigated during two rainy seasons (July to October, 2005 and July to November, 2006) in the villages of Soumousso and Vallée du Kou (VK7). Although the habitats of these villages differ markedly, sympatric populations of M and S molecular forms of An. gambiae s.s. occur in both places periodically. The main aim was to assess the degree to which these molecular forms mate assortatively. In Soumousso, a wooded savannah habitat, the majority of swarm samples consisted of only S-form males (21/28), although a few M-form males were found in mixed M- and S-form swarms. In VK7, a rice growing area, the majority of swarm samples consisted of only M-form males (38/62), until October and November 2006, when there were nearly as many mixed-form as single-form swarms. Overall, ∼60% of M- and S-form swarms were temporally or spatially segregated; the two forms were effectively prevented from encountering each other. Of the remaining 40% of swarms, however, only about half were single-form and the rest were mixed-form. Of the 33 copulae collected from mixed-form swarms, only four were mixed-form pairs, significantly fewer than expected by random pairing between forms (χ(2) = 10.34, d.f. = 2, P < 0.01). Finally, all specimens of inseminated females were of the same form as the sperm contained within their spermatheca (n = 91), even for the four mixed-form copulae. These findings indicate that assortative mating occurs within mixed-form swarms, mediated most probably by close-range mate recognition cues.
    Medical and Veterinary Entomology 01/2013; DOI:10.1111/j.1365-2915.2012.01049.x · 2.33 Impact Factor
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    ABSTRACT: Anopheles gambiae mates in flight. Males gather at stationary places at sunset and compete for incoming females. Factors that account for male mating success are not known but are critical for the future of any genetic control strategy. The current study explored variations in nutritional reserves (sugars, glycogen, lipids, and proteins) in wild-caught swarming and resting males and evaluated the effect of body size and wing symmetry on male mating success. Our results showed that glycogen and sugar reserves are mobilized for flight. Males consume proportionally 5.9-fold as much energy derived from sugars in swarming activities than when they are at rest. Mated males were on average bigger than unmated ones (P<0.0001). A strong correlation between the left and right wings in both mated and unmated males was found and additional analysis on fluctuating asymmetry did not show any indication of mated males being more symmetrical than unmated ones. The distribution of wing size of mated males was focused around a central value, suggesting that intermediate size of males is advantageous in the An. gambiae mating system. The results are discussed in the context of sexual selection.
    Journal of Vector Ecology 12/2012; 37(2):289-97. DOI:10.1111/j.1948-7134.2012.00230.x · 1.44 Impact Factor
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    ABSTRACT: BACKGROUND: The African malaria mosquito, Anopheles gambiae, depends on availability of suitable surface water for oviposition. Short and long dry spells occur throughout the year in many parts of its range that limit its access to oviposition sites. Although not well understood, oviposition-site deprivation has been found to rapidly reduce egg batch size and hatch rate of several mosquito species. We conducted laboratory experiments to assess these effects of oviposition-site deprivation on An. gambiae and to evaluate the role of nutrition and sperm viability as mediators of these effects. METHODS: Anopheles gambiae adults (1--2 d old) from the G3 laboratory colony were assigned to the following treatment groups: oviposition-deprived (fed once and then deprived of oviposition site for 7 or 14 d), multiple-fed control (fed regularly once a week and allowed to lay eggs without delay), and age matched blood-deprived control (fed once, three days before water for oviposition was provided). Egg batch size and hatch rate were measured. In the second experiment two additional treatment groups were included: oviposition-deprived females that received either a second (supplemental) blood meal or virgin males (supplemental mating) 4 days prior to receiving water for oviposition. RESULTS: An. gambiae was highly sensitive to oviposition-site deprivation. Egg batch size dropped sharply to 0--3.5 egg/female within 14 days, due to reduced oviposition rate rather than a reduced number of eggs/batch. Egg hatch rate also fell dramatically to 0-2% within 7 days. The frequency of brown eggs that fail to tan was elevated. A supplemental blood meal, but not 'supplemental insemination,' recovered the oviposition rate of females subjected to oviposition-site deprivation. Similarly, a supplemental blood meal, but not 'supplemental insemination,' partly recovered hatch rate, but this increase was marginally significant (P < 0.069). CONCLUSIONS: Even a short dry spell resulting in oviposition-site deprivation for several days may result in a dramatic decline of An. gambiae populations via reduced fecundity and fertility. However, females taking supplemental blood meals regain at least some reproductive success. If mosquitoes subjected to oviposition-site deprivation increase the frequency of blood feeding, malaria transmission may even increase during a short dry spell. The relevance of oviposition-site deprivation as a cue to alter the physiology of An. gambiae during the long dry season is not evident from these results because no reduction in hatch rate was evident in wild M-form An. gambiae collected in the dry season in the Sahel by previous studies.
    Parasites & Vectors 10/2012; 5(1):235. DOI:10.1186/1756-3305-5-235 · 3.25 Impact Factor
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    ABSTRACT: Malaria 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 eco-physiological changes associated with dry season survival, we measured body size, flight activity and metabolic rate of wild-caught mosquitoes throughout 1 year 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.
    Journal of Experimental Biology 06/2012; 215(Pt 12):2013-21. DOI:10.1242/jeb.069468 · 3.00 Impact Factor
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    ABSTRACT: We describe a novel tracking system for reconstructing three-dimensional tracks of individual mosquitoes in wild swarms and present the results of validating the system by filming swarms and mating events of the malaria mosquito Anopheles gambiae in Mali. The tracking system is designed to address noisy, low frame-rate (25 frames per second) video streams from a stereo camera system. Because flying A. gambiae move at 1-4 m s(-1), they appear as faded streaks in the images or sometimes do not appear at all. We provide an adaptive algorithm to search for missing streaks and a likelihood function that uses streak endpoints to extract velocity information. A modified multi-hypothesis tracker probabilistically addresses occlusions and a particle filter estimates the trajectories. The output of the tracking algorithm is a set of track segments with an average length of 0.6-1 s. The segments are verified and combined under human supervision to create individual tracks up to the duration of the video (90 s). We evaluate tracking performance using an established metric for multi-target tracking and validate the accuracy using independent stereo measurements of a single swarm. Three-dimensional reconstructions of A. gambiae swarming and mating events are presented.
    Journal of The Royal Society Interface 05/2012; 9(75):2624-38. DOI:10.1098/rsif.2012.0150 · 3.86 Impact Factor
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    ABSTRACT: 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.
    Journal of insect physiology 05/2012; 58(8):1050-9. DOI:10.1016/j.jinsphys.2012.04.002 · 2.50 Impact Factor
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    ABSTRACT: We describe an automated tracking system that allows us to reconstruct the 3D kinematics of individual mosquitoes in swarms of Anopheles gambiae. The inputs to the tracking system are video streams recorded from a stereo camera system. The tracker uses a two-pass procedure to automatically localize and track mosquitoes within the swarm. A human-in-the-loop step verifies the estimates and connects broken tracks. The tracker performance is illustrated using footage of mating events filmed in Mali in August 2010.
    Conference proceedings: ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference 08/2011; 2011:720-3. DOI:10.1109/IEMBS.2011.6090163
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    ABSTRACT: In the Sahel, the Anopheles gambiae complex consists of Anopheles arabiensis and the M and S molecular forms of A. gambiae sensu stricto. However, the composition of these malaria vectors varies spatially and temporally throughout the region and is thought to be linked to environmental factors such as rainfall, larval site characteristics and duration of the dry season. To examine possible physiological divergence between these taxa, we measured metabolic rates of mosquitoes during the wet season in a Sahelian village in Mali. To our knowledge, this study provides the first measurements of metabolic rates of A. gambiae and A. arabiensis in the field. The mean metabolic rate of A. arabiensis was higher than that of M-form A. gambiae when accounting for the effects of female gonotrophic status, temperature and flight activity. However, after accounting for their difference in body size, no significant difference in metabolic rate was found between these two species (whilst all other factors were found to be significant). Thus, body size may be a key character that has diverged in response to ecological differences between these two species. Alternatively, these species may display additional differences in metabolic rate only during the dry season. Overall, our results indicate that changes in behavior and feeding activity provide an effective mechanism for mosquitoes to reduce their metabolic rate, and provide insight into the possible strategies employed by aestivating individuals during the dry season. We hypothesize that female mosquitoes switch to sugar feeding while in dormancy because of elevated metabolism associated with blood digestion.
    Journal of Experimental Biology 07/2011; 214(Pt 14):2345-53. DOI:10.1242/jeb.054668 · 3.00 Impact Factor
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    ABSTRACT: Anopheles 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. 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 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. 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 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.
    BMC Evolutionary Biology 06/2011; 11:184. DOI:10.1186/1471-2148-11-184 · 3.41 Impact Factor
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    ABSTRACT: Vector susceptibility to Plasmodium infection is treated primarily as a vector trait, although it is a composite trait expressing the joint occurrence of the parasite and the vector with genetic contributions of both. A comprehensive approach to assess the specific contribution of genetic and environmental variation on "vector susceptibility" is lacking. Here we developed and implemented a simple scheme to assess the specific contributions of the vector, the parasite, and the environment to "vector susceptibility." To the best of our knowledge this is the first study that employs such an approach. We conducted selection experiments on the vector (while holding the parasite "constant") and on the parasite (while holding the vector "constant") to estimate the genetic contributions of the mosquito and the parasite to the susceptibility of Anopheles stephensi to Plasmodium gallinaceum. We separately estimated the realized heritability of (i) susceptibility to parasite infection by the mosquito vector and (ii) parasite compatibility (transmissibility) with the vector while controlling the other. The heritabilities of vector and the parasite were higher for the prevalence, i.e., fraction of infected mosquitoes, than the corresponding heritabilities of parasite load, i.e., the number of oocysts per mosquito. The vector's genetics (heritability) comprised 67% of "vector susceptibility" measured by the prevalence of mosquitoes infected with P. gallinaceum oocysts, whereas the specific contribution of parasite genetics (heritability) to this trait was only 5%. Our parasite source might possess minimal genetic diversity, which could explain its low heritability (and the high value of the vector). Notably, the environment contributed 28%. These estimates are relevant only to the particular system under study, but this experimental design could be useful for other parasite-host systems. The prospects and limitations of the genetic manipulation of vector populations to render the vector resistant to the parasite are better considered on the basis of this framework.
    PLoS ONE 06/2011; 6(6):e20156. DOI:10.1371/journal.pone.0020156 · 3.53 Impact Factor
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    ABSTRACT: Persistence 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. To 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. The 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. These 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.
    Malaria Journal 06/2011; 10:151. DOI:10.1186/1475-2875-10-151 · 3.49 Impact Factor
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    ABSTRACT: 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.
    The American journal of tropical medicine and hygiene 09/2010; 83(3):601-6. DOI:10.4269/ajtmh.2010.09-0779 · 2.74 Impact Factor
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    ABSTRACT: Reduced survival and future reproduction due to of current reproduction is a trade-off known as the cost of reproduction. Surprisingly, only a few studies have assessed the cost of reproduction in arthropod disease vectors, despite its effect on longevity, and thus on vectorial capacity. We evaluated the cost of reproduction on survival of Anopheles gambiae Giles by comparing mosquitoes that were denied exposure to the other sex, hereafter named virgins, and those that were allowed exposure to the other sex and mating, hereafter named mated. Merely 6 d of exposure to females with mating activity reduced male survival from a median of 17 d in virgins to 15 d in mated, indicating that male mating cost is substantial. The increase in mortality of mated males began several days after the exposure to females ended, indicating that mating is not associated with immediate mortality risk. Notably, body size was negatively correlated with male mortality in mated males, but not in virgins. The rate of insemination declined after 4 d of exposure to females, indicating that male mating capacity is limited and further supporting the hypothesis that mating is costly for males. Consistent with previous studies, female survival on sugar alone (median=16 d) was shorter than on blood and sugar (median=19 d), regardless if she was mated or virgin. Overall, survival of mated females was lower than that of virgins on a diet of blood and sugar, but no difference was found on a diet of sugar only. However, the cost of reproduction in females remains ambiguous because the difference in survival between virgin and mated females was driven by the difference between virgin (median=19 d) and uninseminated females exposed to males (median=17 d), rather than between virgin and inseminated females (median=19 d). Accordingly, sperm and seminal fluid, egg development, and oviposition have negligible cost in terms of female survival. Only exposure to males without insemination decreased female survival. Nonetheless, if exposure to males under natural conditions is also associated with reduced survival, it might explain why females remain monogamous.
    Journal of Medical Entomology 09/2010; 47(5):769-77. DOI:10.1603/ME10052 · 1.82 Impact Factor
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    ABSTRACT: Anopheles gambiae, the major malaria vector in Africa, can be divided into two subgroups based on genetic and ecological criteria. These two subgroups, termed the M and S molecular forms, are believed to be incipient species. Although they display differences in the ecological niches they occupy in the field, they are often sympatric and readily hybridize in the laboratory to produce viable and fertile offspring. Evidence for assortative mating in the field was recently reported, but the underlying mechanisms awaited discovery. We studied swarming behaviour of the molecular forms and investigated the role of swarm segregation in mediating assortative mating. Molecular identification of 1145 males collected from 68 swarms in Donéguébougou, Mali, over 2 years revealed a strict pattern of spatial segregation, resulting in almost exclusively monotypic swarms with respect to molecular form. We found evidence of clustering of swarms composed of individuals of a single molecular form within the village. Tethered M and S females were introduced into natural swarms of the M form to verify the existence of possible mate recognition operating within-swarm. Both M and S females were inseminated regardless of their form under these conditions, suggesting no within-mate recognition. We argue that our results provide evidence that swarm spatial segregation strongly contributes to reproductive isolation between the molecular forms in Mali. However this does not exclude the possibility of additional mate recognition operating across the range distribution of the forms. We discuss the importance of spatial segregation in the context of possible geographic variation in mechanisms of reproductive isolation.
    Proceedings of the Royal Society B: Biological Sciences 10/2009; 276(1676):4215-22. DOI:10.1098/rspb.2009.1167 · 5.29 Impact Factor

Publication Stats

4k Citations
293.02 Total Impact Points

Institutions

  • 2007–2014
    • National Institute of Allergy and Infectious Diseases
      Maryland, United States
    • National Institute of Allergy and Infectious Disease
      Роквилл, Maryland, United States
  • 2006–2014
    • National Institutes of Health
      • Laboratory of Malaria and Vector Research Molecular Immunology
      베서스다, Maryland, United States
    • University of the Andes (Chile)
      CiudadSantiago, Santiago Metropolitan, Chile
    • Research Institute of Health Sciences
      Wagadugu, Centre, Burkina Faso
    • University of Peradeniya
      • Department of Veterinary Pathobiology
      Mahanuvara, Central, Sri Lanka
  • 2000–2009
    • Emory University
      • Department of Biology
      Atlanta, Georgia, United States
    • Institute of Research for Development
      Marsiglia, Provence-Alpes-Côte d'Azur, France
  • 2008
    • National Eye Institute
      Maryland, United States
  • 1996–2006
    • Centers for Disease Control and Prevention
      • Division of Parasitic Diseases and Malaria
      Atlanta, MI, United States
  • 2004–2005
    • United States Department of Agriculture
      • Agricultural Research Service (ARS)
      Washington, D. C., DC, United States
    • Justus-Liebig-Universität Gießen
      • Institute of Animal Nutrition and Nutritional Physiology
      Gieben, Hesse, Germany
  • 2003
    • Cairo University
      • Department of Parasitology
      Al Qāhirah, Al Qāhirah, Egypt
    • Natural Resources Research Institute
      Silver Spring, Maryland, United States
    • Universidade Estadual do Norte Fluminense
      • Center of Biosciences and Biotechnology – CBB
      Rio de Janeiro, Rio de Janeiro, Brazil
  • 2002
    • Washington University in St. Louis
      San Luis, Missouri, United States
    • Liverpool School of Tropical Medicine
      • Vector Group
      Liverpool, ENG, United Kingdom