Dataset Information

Population Structure and Migration Patterns of the Tsetse Fly Glossina fuscipes in Congo-Brazzaville.

ABSTRACT: Tsetse flies of the palpalis group, particularly Glossina fuscipes, are the main vectors of human African trypanosomiasis or sleeping sickness in Congo-Brazzaville. They transmit the deadly human parasite, Trypanosoma brucei gambiense and other trypanosomes that cause animal trypanosomiasis. Knowledge on diversity, population structure, population size, and gene flow is a prerequisite for designing effective tsetse control strategies. There is limited published information on these parameters including migration patterns of G. fuscipes in Congo-Brazzaville. We genotyped 288 samples of G. fuscipes from Bomassa (BMSA), Bouemba (BEMB), and Talangai (TLG) locations at 10 microsatellite loci and determined levels of genetic diversity, differentiation, structuring, and gene flow among populations. We observed high genetic diversity in all three localities. Mean expected heterozygosity was 0.77 ± 0.04, and mean allelic richness was 11.2 ± 1.35. Deficiency of heterozygosity was observed in all populations with positive and significant F IS values (0.077-0.149). Structure analysis revealed three clusters with genetic admixtures, evidence of closely related but potentially different taxa within G. fuscipes. Genetic differentiation indices were low but significant (F ST = 0.049, P < 0.05), indicating ongoing gene flow countered with a stronger force of drift. We recorded significant migration from all the three populations, suggesting exchange of genetic information between and among locations. Ne estimates revealed high and infinite population sizes in BEMB and TLG. These critical factors should be considered when planning area-wide tsetse control interventions in the country to prevent resurgence of tsetse from relict populations and/or reinvasion of cleared habitats.

SUBMITTER: Mayoke A

PROVIDER: S-EPMC7941806 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Population Structure and Migration Patterns of the Tsetse Fly Glossina fuscipes in Congo-Brazzaville.

Mayoke Abraham A Ouma Johnson O JO Mireji Paul O PO Omondi Stephen F SF Muya Shadrack M SM Itoua Andre A Okoth Sylvance O SO Bateta Rosemary R

The American journal of tropical medicine and hygiene 20201228 3

Tsetse flies of the palpalis group, particularly Glossina fuscipes, are the main vectors of human African trypanosomiasis or sleeping sickness in Congo-Brazzaville. They transmit the deadly human parasite, Trypanosoma brucei gambiense and other trypanosomes that cause animal trypanosomiasis. Knowledge on diversity, population structure, population size, and gene flow is a prerequisite for designing effective tsetse control strategies. There is limited published information on these parameters in ...[more]

PMID: 33372648

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Project description:Uganda is the only country where the chronic and acute forms of human African Trypanosomiasis (HAT) or sleeping sickness both occur and are separated by < 100 km in areas north of Lake Kyoga. In Uganda, Glossina fuscipes fuscipes is the main vector of the Trypanosoma parasites responsible for these diseases as well for the animal African Trypanosomiasis (AAT), or Nagana. We used highly polymorphic microsatellite loci and a mitochondrial DNA (mtDNA) marker to provide fine scale spatial resolution of genetic structure of G. f. fuscipes from 42 sampling sites from the northern region of Uganda where a merger of the two disease belts is feared. Based on microsatellite analyses, we found that G. f. fuscipes in northern Uganda are structured into three distinct genetic clusters with varying degrees of interconnectivity among them. Based on genetic assignment and spatial location, we grouped the sampling sites into four genetic units corresponding to northwestern Uganda in the Albert Nile drainage, northeastern Uganda in the Lake Kyoga drainage, western Uganda in the Victoria Nile drainage, and a transition zone between the two northern genetic clusters characterized by high level of genetic admixture. An analysis using HYBRIDLAB supported a hybrid swarm model as most consistent with tsetse genotypes in these admixed samples. Results of mtDNA analyses revealed the presence of 30 haplotypes representing three main haplogroups, whose location broadly overlaps with the microsatellite defined clusters. Migration analyses based on microsatellites point to moderate migration among the northern units located in the Albert Nile, Achwa River, Okole River, and Lake Kyoga drainages, but not between the northern units and the Victoria Nile drainage in the west. Effective population size estimates were variable with low to moderate sizes in most populations and with evidence of recent population bottlenecks, especially in the northeast unit of the Lake Kyoga drainage. Our microsatellite and mtDNA based analyses indicate that G. f. fuscipes movement along the Achwa and Okole rivers may facilitate northwest expansion of the Rhodesiense disease belt in Uganda. We identified tsetse migration corridors and recommend a rolling carpet approach from south of Lake Kyoga northward to minimize disease dispersal and prevent vector re-colonization. Additionally, our findings highlight the need for continuing tsetse monitoring efforts during and after control.

Project description:BackgroundGlossina fuscipes fuscipes, a riverine species of tsetse, is the main vector of both human and animal trypanosomiasis in Uganda. Successful implementation of vector control will require establishing an appropriate geographical scale for these activities. Population genetics can help to resolve this issue by characterizing the extent of linkage among apparently isolated groups of tsetse.Methodology/principal findingsWe conducted genetic analyses on mitochondrial and microsatellite data accumulated from approximately 1000 individual tsetse captured in Uganda and neighboring regions of Kenya and Sudan. Phylogeographic analyses suggested that the largest scale genetic structure in G. f. fuscipes arose from an historical event that divided two divergent mitochondrial lineages. These lineages are currently partitioned to northern and southern Uganda and co-occur only in a narrow zone of contact extending across central Uganda. Bayesian assignment tests, which provided evidence for admixture between northern and southern flies at the zone of contact and evidence for northerly gene flow across the zone of contact, indicated that this structure may be impermanent. On the other hand, microsatellite structure within the southern lineage indicated that gene flow is currently limited between populations in western and southeastern Uganda. Within regions, the average F(ST) between populations separated by less than 100 km was less than approximately 0.1. Significant tests of isolation by distance suggested that gene flow is ongoing between neighboring populations and that island populations are not uniformly more isolated than mainland populations.Conclusions/significanceDespite the presence of population structure arising from historical colonization events, our results have revealed strong signals of current gene flow within regions that should be accounted for when planning tsetse control in Uganda. Populations in southeastern Uganda appeared to receive little gene flow from populations in western or northern Uganda, supporting the feasibility of area wide control in the Lake Victoria region by the Pan African Tsetse and Trypanosomiasis Eradication Campaign.

Project description:Tsetse flies (Glossina spp.) are vectors of parasitic trypanosomes, which cause human (HAT) and animal African trypanosomiasis (AAT) in sub-Saharan Africa. In Uganda, Glossina fuscipes fuscipes (Gff) is the main vector of HAT, where it transmits Gambiense disease in the northwest and Rhodesiense disease in central, southeast and western regions. Endosymbionts can influence transmission efficiency of parasites through their insect vectors via conferring a protective effect against the parasite. It is known that the bacterium Spiroplasma is capable of protecting its Drosophila host from infection with a parasitic nematode. This endosymbiont can also impact its host's population structure via altering host reproductive traits. Here, we used field collections across 26 different Gff sampling sites in northern and western Uganda to investigate the association of Spiroplasma with geographic origin, seasonal conditions, Gff genetic background and sex, and trypanosome infection status. We also investigated the influence of Spiroplasma on Gff vector competence to trypanosome infections under laboratory conditions. Generalized linear models (GLM) showed that Spiroplasma probability was correlated with the geographic origin of Gff host and with the season of collection, with higher prevalence found in flies within the Albert Nile (0.42 vs 0.16) and Achwa River (0.36 vs 0.08) watersheds and with higher prevalence detected in flies collected in the intermediate than wet season. In contrast, there was no significant correlation of Spiroplasma prevalence with Gff host genetic background or sex once geographic origin was accounted for in generalized linear models. Additionally, we found a potential negative correlation of Spiroplasma with trypanosome infection, with only 2% of Spiroplasma infected flies harboring trypanosome co-infections. We also found that in a laboratory line of Gff, parasitic trypanosomes are less likely to colonize the midgut in individuals that harbor Spiroplasma infection. These results indicate that Spiroplasma infections in tsetse may be maintained by not only maternal but also via horizontal transmission routes, and Spiroplasma infections may also have important effects on trypanosome transmission efficiency of the host tsetse. Potential functional effects of Spiroplasma infection in Gff could have impacts on vector control approaches to reduce trypanosome infections.

Project description:Wolbachia pipientis, a diverse group of ?-proteobacteria, can alter arthropod host reproduction and confer a reproductive advantage to Wolbachia-infected females (cytoplasmic incompatibility (CI)). This advantage can alter host population genetics because Wolbachia-infected females produce more offspring with their own mitochondrial DNA (mtDNA) haplotypes than uninfected females. Thus, these host haplotypes become common or fixed (selective sweep). Although simulations suggest that for a CI-mediated sweep to occur, there must be a transient phase with repeated initial infections of multiple individual hosts by different Wolbachia strains, this has not been observed empirically. Wolbachia has been found in the tsetse fly, Glossina fuscipes fuscipes, but it is not limited to a single host haplotype, suggesting that CI did not impact its population structure. However, host population genetic differentiation could have been generated if multiple Wolbachia strains interacted in some populations. Here, we investigated Wolbachia genetic variation in G. f. fuscipes populations of known host genetic composition in Uganda. We tested for the presence of multiple Wolbachia strains using Multi-Locus Sequence Typing (MLST) and for an association between geographic region and host mtDNA haplotype using Wolbachia DNA sequence from a variable locus, groEL (heat shock protein 60).MLST demonstrated that some G. f. fuscipes carry Wolbachia strains from two lineages. GroEL revealed high levels of sequence diversity within and between individuals (Haplotype diversity = 0.945). We found Wolbachia associated with 26 host mtDNA haplotypes, an unprecedented result. We observed a geographical association of one Wolbachia lineage with southern host mtDNA haplotypes, but it was non-significant (p = 0.16). Though most Wolbachia-infected host haplotypes were those found in the contact region between host mtDNA groups, this association was non-significant (p = 0.17).High Wolbachia sequence diversity and the association of Wolbachia with multiple host haplotypes suggest that different Wolbachia strains infected G. f. fuscipes multiple times independently. We suggest that these observations reflect a transient phase in Wolbachia evolution that is influenced by the long gestation and low reproductive output of tsetse. Although G. f. fuscipes is superinfected with Wolbachia, our data does not support that bidirectional CI has influenced host genetic diversity in Uganda.

Dataset Information

Population Structure and Migration Patterns of the Tsetse Fly Glossina fuscipes in Congo-Brazzaville.

Publications

Population Structure and Migration Patterns of the Tsetse Fly Glossina fuscipes in Congo-Brazzaville.

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