Browsing by Author "Dion, Kirstin"

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    Evidence of temporal stability in allelic and mitochondrial haplotype diversity in populations of Glossina fuscipes fuscipes (Diptera: Glossinidae) in northern Uganda
    (Parasites & Vectors, 2016) Opiro, Robert; Saarman, Norah P.; Echodu, Richard; Opiyo, Elizabeth A.; Dion, Kirstin; Halyard, Alexis; Aksoy, Serap; Caccone, Adalgisa
    Glossina fuscipes fuscipes is a tsetse species of high economic importance in Uganda where it is responsible for transmitting animal African trypanosomiasis (AAT) and both the chronic and acute forms of human African trypanosomiasis (HAT). We used genotype data from 17 microsatellites and a mitochondrial DNA marker to assess temporal changes in gene frequency for samples collected between the periods ranging from 2008 to 2014 in nine localities spanning regions known to harbor the two forms of HAT in northern Uganda. Results: Our findings suggest that the majority of the studied populations in both HAT foci are genetically stable across the time span sampled. Pairwise estimates of differentiation using standardized FST and Jost’s DEST between time points sampled for each site were generally low and ranged between 0.0019 and 0.1312 for both sets of indices. We observed the highest values of FST and DEST between time points sampled from Kitgum (KT), Karuma (KR), Moyo (MY) and Pader (PD), and the possible reasons for this are discussed. Effective population size (Ne) estimates using Waple’s temporal method ranged from 103 (95 % CI: 73–138) in Kitgum to 962 (95 % CI: 669–1309) in Oculoi (OC). Additionally, evidence of a bottleneck event was detected in only one population at one time point sampled; Aminakwach (AM-27) from December 2014 (P < 0.03889). Conclusion: Findings suggest general temporal stability of tsetse vectors in foci of both forms of HAT in northern Uganda. Genetic stability and the moderate effective population sizes imply that a re-emergence of vectors from local residual populations missed by control efforts is an important risk. This underscores the need for more sensitive sampling and monitoring to detect residual populations following control activities.
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    Genetic diversity and population structure of the tsetse fly Glossina fuscipes fuscipes (Diptera: Glossinidae) in Northern Uganda: Implications for vector control
    (PLOS Neglected Tropical Diseases, 2017) Opiro, Robert; Saarman, Norah P.; Echodu, Richard; Opiyo, Elizabeth A.; Dion, Kirstin; Halyard, Alexis; Dunn, Augustine W.; Aksoy, Serap; Caccone, Adalgisa
    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.
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    The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda
    (Saarman, N. P., Opiro, R., Hyseni, C., Echodu, R., Opiyo, E. A., Dion, K., ... & Caccone, A. (2019). The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda. Molecular ecology, 28(1), 66-85., 2019) Saarman, Norah P.; Opiro, Robert; Hyseni, Chaz; Echodu, Richard; Opiyo, Elizabeth A.; Dion, Kirstin; Johnson, Thomas; Aksoy, Serap; Caccone, Adalgisa
    Understanding the mechanisms that enforce, maintain or reverse the process of speciation is an important challenge in evolutionary biology. This study investigates the patterns of divergence and discusses the processes that form and maintain divergent lineages of the tsetse fly Glossina fuscipes fuscipes in Uganda. We sampled 251 flies from 18 sites spanning known genetic lineages and the four admixture zones between them. We apply population genomics, hybrid zone and approximate Bayesian computation to the analysis of three types of genetic markers: 55,267 double-digest restriction site-associated DNA (ddRAD) SNPs to assess genome-wide admixture, 16 microsatellites to provide continuity with published data and accurate biogeographic modelling, and a 491-bp fragment of mitochondrial cytochrome oxidase I and II to infer maternal inheritance patterns. Admixture zones correspond with regions impacted by the reorganization of Uganda's river networks that occurred during the formation of the West African Rift system over the last several hundred thousand years. Because tsetse fly population distributions are defined by rivers, admixture zones likely represent both old and new regions of secondary contact. Our results indicate that older hybrid zones contain mostly parental types, while younger zones contain variable hybrid types resulting from multiple generations of interbreeding. These findings suggest that reproductive barriers are nearly complete in the older admixture zones, while nearly absent in the younger admixture zones. Findings are consistent with predictions of hybrid zone theory: Populations in zones of secondary contact transition rapidly from early to late stages of speciation or collapse all together.
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    A spatial genetics approach to inform vector control of tsetse flies (Glossina fuscipes fuscipes) in Northern Uganda
    (Ecology and evolution, 2018) Saarman, Norah; Burak, Mary; Opiro, Robert; Hyseni, Chaz; Echodu, Richard; Dion, Kirstin; Opiyo, Elizabeth A.; Dunn, Augustine W.; Amatulli, Giuseppe; Aksoy, Serap; Caccone, Adalgisa
    Tsetse flies (genus Glossina) are the only vector for the parasitic trypanosomes responsible for sleeping sickness and nagana across sub-Saharan Africa. In Uganda, the tsetse fly Glossina fuscipes fuscipes is responsible for transmission of the parasite in 90% of sleeping sickness cases, and co-occurrence of both forms of human-infective trypanosomes makes vector control a priority. We use population genetic data from 38 samples from northern Uganda in a novel methodological pipeline that integrates genetic data, remotely sensed environmental data, and hundreds of field-survey observations. This methodological pipeline identifies isolated habitat by first identifying environmental parameters correlated with genetic differentiation, second, predicting spatial connectivity using field-survey observations and the most predictive environmental parameter(s), and third, overlaying the connectivity surface onto a habitat suitability map. Results from this pipeline indicated that net photosynthesis was the strongest predictor of genetic differentiation in G. f. fuscipes in northern Uganda. The resulting connectivity surface identified a large area of well-connected habitat in northwestern Uganda, and twenty-four isolated patches on the northeastern margin of the G. f. fuscipes distribution. We tested this novel methodological pipeline by completing an ad hoc sample and genetic screen of G. f. fuscipes s amples f rom a m odel-predicted isolated patch, and evaluated whether the ad hoc sample was in fact as genetically isolated as predicted. Results indicated that genetic isolation of the ad hoc sample was as genetically isolated as predicted, with differentiation well above estimates made in samples from within well-connected habitat separated by similar geographic distances. This work has important practical implications for the control of tsetse and other disease vectors, because it provides a way to identify isolated populations where it will be safer and easier to implement vector control and that should be prioritized as study sites during the development and improvement of vector control methods.
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    Spatio-temporal distribution of Spiroplasma infections in the tsetse fly (Glossina fuscipes fuscipes) in northern Uganda
    (PLOS Neglected Tropical Diseases, 2019) Schneider, Daniela I.; Saarman, Norah; Onyango, Maria G.; Hyseni, Chaz; Opiro, Robert; Echodu, Richard; O’Neill, Michelle; Bloch, Danielle; Vigneron, Aure´lien; Johnson, T. J.; Dion, Kirstin; Weiss, Brian L.; Opiyo, Elizabeth; Caccone, Adalgisa; Aksoy, Serap
    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.