Tovi Lehmann

The molecular forms of Anopheles gambiae: a phenotypic perspective.

The African malaria mosquito Anopheles gambiae is undergoing speciation, being split into the M and S molecular forms. Speciation is the main process promoting biological diversity, thus, new vector species might complicate disease transmission. Genetic differentiation between the molecular forms has been extensively studied, but phenotypic differences between them, the evolutionary forces that generated divergence, and the mechanisms that maintain their genetic isolation have only recently been addressed. Here, we review recent studies suggesting that selection mediated by larval predation and competition promoted divergence between temporary and permanent freshwater habitats. These differences explain the sharp discontinuity in distribution of the molecular forms between rice fields and surrounding savanna, but they can also explain the concurrent cline between humid and arid environments due to the dependence on permanent habitats in the latter. Although less pronounced, differences in adult body size, reproductive output, and longevity also suggest that the molecular forms have adapted to distinct niches. Reproductive isolation between the molecular forms is achieved by spatial swarm segregation, although within-swarm mate recognition appears to play a role in certain locations. The implications of these results to disease transmission and control are discussed and many of the gaps in our understanding are highlighted.

Revisiting the role of introgression vs shared ancestral polymorphisms as key processes shaping genetic diversity in the recently separated sibling species of the Anopheles gambiae complex.

The role of interspecific hybridisation in the evolution of pest species is poorly understood. In mosquito disease vectors this is of particular importance due to the evolution of insecticide resistance and the proposed release of transgenic strains that are refractory to the malaria parasite. In this study, we apply population genetic methods in a novel manner to determine whether mitochondrial DNA sequences have introgressed between the closely related African malaria vectors Anopheles gambiae and A. arabiensis. Our results suggest that speciation was geologically recent and ancestral haplotypes at the ND5 locus are retained in both species. In addition, comparing haplotype frequencies in allopatric and sympatric populations, suggest locale specific unidirectional introgression of mitochondria from A. arabiensis into A. gambiae.

Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation

BackgroundThe molecular forms of Anopheles gambiae are undergoing speciation. They are characterized by a strong assortative mating and they display partial habitat segregation. The M form is mostly found in flooded/irrigated areas whereas the S form dominates in the surrounding areas, but the ecological factors that shape this habitat segregation are not known. Resource competition has been demonstrated between species undergoing divergent selection, but resource competition is not the only factor that can lead to divergence.ResultsIn a field experiment using transplantation of first instar larvae, we evaluated the role of larval predators in mediating habitat segregation between the forms. We found a significant difference in the ability of the molecular forms to exploit the different larval sites conditioned on the presence of predators. In absence of predation, the molecular forms outcompeted each other in their respective natural habitats however, the developmental success of the M form was significantly higher than that of the S form in both habitats under predator pressure.ConclusionOur results provide the first empirical evidence for specific adaptive differences between the molecular forms and stress the role of larval predation as one of the mechanisms contributing to their divergence.

Mixed swarms of the molecular M and S forms of Anopheles gambiae (Diptera : Culicidae) in sympatric area from Burkina Faso

Abstract The M and S molecular forms of Anopheles gambiae sensu stricto Giles are thought to be reproductively isolated through premating barriers. However, the exact mechanisms of recognition of conspecific partners are unknown. Because mating in An. gambiae occurs in swarms, one might expect swarming behavior between the M and S forms to be different and that this probably reduces the risk of contact between males and females of the different forms in areas where they are sympatric. We report the occurrence of four mixed swarms, containing males of M and S forms, out of a total of 26 swarms sampled in Soumousso, a typical savannah village of Burkina Faso, West Africa. However, the frequency of mixed swarms was lower than that expected by chance. This observation suggests partial segregation between the swarms of the molecular forms, which may contribute to their isolation. Because the frequency of mixed swarms seems too high to explain the low frequency of cross-mating and hybrids, we suggest that mate recognition in a swarm is more important than swarm segregation.

Evaluating the Effect of Postmating Isolation Between Molecular Forms of Anopheles gambiae (Diptera: Culicidae)

Abstract Multiple families representing all possible combinations of crosses between the two molecular forms of Anopheles gambiae sensu stricto Giles and their hybrids were set up using forced mating between offspring of wild-collected females. The results showed that the reproductive output of hybrids and their backcrosses was similar to that of the pure forms as measured by egg batch size, hatching rate, and larval development success. No sex ratio distortion was found among the offspring. We concluded that postmating developmental barriers do not contribute to the isolation between the molecular forms.

Spatial distribution and male mating success of Anopheles gambiae swarms

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.

The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel

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.

Structure and Dynamics of Male Swarms of Anopheles gambiae

ABSTRACT 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 in dividual 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 afemale or aproduct 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.

The distribution of hatching time in Anopheles gambiae

BackgroundKnowledge of the ecological differences between the molecular forms of Anopheles gambiae and their sibling species, An. arabiensis might lead to understanding their unique contribution to disease transmission and to better vector control as well as to understanding the evolutionary forces that have separated them.MethodsThe distributions of hatching time of eggs of wild An. gambiae and An. arabiensis females were compared in different water types. Early and late hatchers of the S molecular form were compared with respect to their total protein content, sex ratio, development success, developmental time and adult body size.ResultsOverall, the distribution of hatching time was strongly skewed to the right, with 89% of the eggs hatching during the second and third day post oviposition, 10% hatching during the next four days and the remaining 1% hatching over the subsequent week. Slight, but significant differences were found between species and between the molecular forms in all water types. Differences in hatching time distribution were also found among water types (in each species and molecular form), suggesting that the eggs change their hatching time in response to chemical factors in the water. Early hatchers were similar to late hatchers except that they developed faster and produced smaller adults than late hatchers.ConclusionDifferences in hatching time and speed of development among eggs of the same batch may be adaptive if catastrophic events such as larval site desiccation are not rare and the sites quality is unpredictable. The egg is not passive and its hatching time depends on water factors. Differences in hatching time between species and molecular forms were slight, probably reflecting that conditions in their larval sites are rather similar.

Dry season reproductive depression of Anopheles gambiae in the Sahel

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.