High Levels of Genetic Differentiation between Ugandan Glossina fuscipes fuscipes Populations Separated by Lake Kyoga

Abstract

Glossina fuscipes fuscipes is the major vector of human African trypanosomiasis, commonly referred to as sleeping sickness, in Uganda. In western and eastern Africa, the disease has distinct clinical manifestations and is caused by two different parasites: Trypanosoma brucei rhodesiense and T. b. gambiense. Uganda is exceptional in that it harbors both parasites, which are separated by a narrow 160-km belt. This separation is puzzling considering there are no restrictions on the movement of people and animals across this region. We investigated whether genetic heterogeneity of G. f. fuscipes vector populations can provide an explanation for this disjunct distribution of the Trypanosoma parasites. Therefore, we examined genetic structuring of G. f. fuscipes populations across Uganda using newly developed microsatellite markers, as well as mtDNA. Our data show that G. f. fuscipes populations are highly structured, with two clearly defined clusters that are separated by Lake Kyoga, located in central Uganda. Interestingly, we did not find a correlation between genetic heterogeneity and the type of Trypanosoma parasite transmitted. The lack of a correlation between genetic structuring of G. f. fuscipes populations and the distribution of T. b. gambiense and T. b. rhodesiense indicates that it is unlikely that genetic heterogeneity of G. f. fuscipes populations explains the disjunct distribution of the parasites. These results have important epidemiological implications, suggesting that a fusion of the two disease distributions is unlikely to be prevented by an incompatibility between vector populations and parasite. The two types of sleeping sickness in West and East Africa are markedly distinct, require different treatments, and are caused by different parasites. The only country where both parasites are present is Uganda, where they are separated by a narrow 160 km disease-free belt. Because there is no restriction on the movement of humans and animals between the two disease zones, this separation is puzzling. We asked whether this disjunct distribution can be explained by variation within the tsetse fly that is largely responsible for transmitting both diseases in Uganda, Glossina fuscipes fuscipes. We therefore examined whether this tsetse subspecies is genetically uniform across Uganda. Our results indicate that G. f. fusicipes is not genetically different between the two disease zones, but there are clear genetic differences between northern and southern populations, which are separated by Lake Kyoga. Therefore, it is unlikely that variation in the tsetse fly determines the distribution of the two parasites. This implies that the two diseases may fuse in the near future, which would greatly complicate diagnosis and treatment of sleeping sickness in any potential area of overlap.