Toxoplasma gondii is a protozoan parasite that infects nearly all mammal and bird species worldwide. Usually asymptomatic, toxoplasmosis can be severe and even fatal to many hosts, including people. Elucidating the contribution of genetic variation among parasites to patterns of disease transmission and manifestations has been the goal of many studies. Focusing on the geographic component of this variation, we show that most genotypes are locale-specific, but some are found across continents and are closely related to each other, indicating a recent radiation of a pandemic genotype. Furthermore, we show that the geographic structure of T. gondii is extraordinary in having one population that is found in all continents except South America, whereas other populations are generally confined to South America, and yet another population is found worldwide. Our evidence suggests that South American and Eurasian populations have evolved separately until recently, when ships populated by rats, mice, and cats provided T. gondii with unprecedented migration opportunities, probably during the transatlantic slave trade. Our results explain several enigmatic features of the population structure of T. gondii and demonstrate how pervasive, prompt, and elusive the impact of human globalization is on nature.evolutionary history ͉ migration ͉ pandemic genotype ͉ protozoan parasite ͉ trade

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

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Attempts to reconstruct the phylogenetic history of the Anopheles gambiae cryptic species complex have yielded strongly conflicting results. In particular, An. gambiae, the primary African malaria vector, is variously placed as a sister taxon to either Anopheles arabiensis or Anopheles merus. The recent divergence times for members of this complex complicate phylogenetic analysis, making it difficult to unambiguously implicate interspecific gene flow, versus retained ancestral polymorphism, as the source of conflict. Using sequences at four unlinked loci, which were determined from multiple specimens within each of five species in the complex, we found contrasting patterns of sequence divergence between the X chromosome and the autosomes. The isolation model of speciation assumes a lack of gene flow between species since their separation. This model could not be rejected for An. gambiae and An. arabiensis, although the data fit the model poorly. On the other hand, evidence from gene trees supports genetic introgression of chromosome 2 inversions between An. gambiae and An. arabiensis, and also points to more broad scale genetic exchange of autosomal sequences between this species pair. That such exchange has been relatively recent is suggested not only by the lack of fixed differences at three autosomal loci but also by the sharing of full haplotypes at two of the three loci, which is in contrast to several fixed differences and considerably deeper divergence on the X. The proposed acquisition by An. gambiae of sequences from the more arid-adapted An. arabiensis may have contributed to the spread and ecological dominance of this malaria vector.

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.

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The population structure of Anopheles gambiae in Africa was studied using 11 microsatellite loci in 16 samples from 10 countries. All loci are located outside polymorphic inversions. Heterogeneity among loci was detected and two putative outlier loci were removed from analyses aimed at capturing genome-wide patterns. Two main divisions of the gene pool were separated by high differentiation (F(ST) > 0.1). The northwestern (NW) division included populations from Senegal, Ghana, Nigeria, Cameroon, Gabon, Democratic Republic of Congo (DRC), and western Kenya. The southeastern (SE) division included populations from eastern Kenya, Tanzania, Malawi, and Zambia. Inhospitable environments for A. gambiae along the Rift Valley partly separate these divisions. Reduced genetic diversity in the SE division and results of an analysis based on private alleles support the hypothesis that a recent bottleneck, followed by colonization from the NW populations shaped this structure. In the NW division, populations possessing the M rDNA genotype appeared to form a monophyletic clade. Although genetic distance increased with geographic distance, discontinuities were suggested between certain sets of populations. The absence of heterozygotes between sympatric M and S populations in the DRC and the high differentiation in locus 678 (F(ST)>0.28) contrasted with low differentiation in all other loci (-0.02

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.