Browsing by Author "Opiyo, Elizabeth A."
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Item 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, AdalgisaGlossina 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.Item 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, AdalgisaUganda 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.Item Heterogeneity in the prevalence and intensity of bovine trypanosomiasis in the districts of Amuru and Nwoya, Northern Uganda(BMC veterinary research, 2015) Angwech, Harriet; Nyeko, Jack H. P.; Opiyo, Elizabeth A.; Okello-Onen, Joseph; Opiro, Robert; Echodu, Richard; Malinga, Geoffrey M.; Njahira, Moses N.; Skilton, Robert A.Livestock trypanosomiasis, transmitted mainly by tsetse flies of the genus Glossina is a major constraint to livestock health and productivity in the sub-Saharan Africa. Knowledge of the prevalence and intensity of trypanosomiasis is important in understanding the epidemiology of the disease. The objectives of this study were to (a) assess the prevalence and intensity of trypanosome infections in cattle, and (b) to investigate the reasons for the heterogeneity of the disease in the tsetse infested districts of Amuru and Nwoya, northern Uganda. Methods: A cross-sectional study was conducted from September, 2011 to January, 2012. Blood samples were collected from 816 cattle following jugular vein puncture, and screened for trypanosomes by HCT and ITS-PCR. A Pearson chi-squared test and logistic regression analyses were performed to determine the association between location, age, sex, and prevalence of trypanosome infections. Results: Out of the 816 blood samples examined, 178 (22 %) and 338 (41 %) tested positive for trypanosomiasis by HCT and ITS-PCR, respectively. Trypanosoma vivax infection accounted for 77 % of infections detected by ITS-PCR, T. congolense (16 %), T. brucei s.l (4 %) and mixed (T. vivax/ T. congolense/T.brucei) infections (3 %). The risk of trypanosome infection was significantly associated with cattle age (χ2 = 220.4, df = 3, P < 0.001). The highest proportions of infected animals were adult males (26.7 %) and the least infected were the less than one year old calves (2.0 %). In addition, the risk of trypanosome infection was significantly associated with sex (χ2 = 16.64, df=1, P < 0.001), and males had a significantly higher prevalence of infections (26.8 %) than females (14.6 %). Conclusion: Our results indicate that the prevalence and intensity of trypanosome infections are highly heterogeneous being associated with cattle age, location and sex.Item High level of resistance in Anopheles arabiensis mosquito to pyrethroid insecticides from low malaria transmission zone of Moroto district, Karamoja region, Uganda: Implication for malaria vector control(Research Square, 2020) Echodu, Richard; Anena, Juliet; Iwiru, Tereza; Mireji, Paul; Malinga, Geoffrey Maxwell; Opiyo, Elizabeth A.; Iga, Julius; David, OnanyangKaramoja region of Uganda previously classified as low malaria transmission zone is currently experiencing significant upsurge of malaria incidences. Long lasting insecticidal nets (LLINs) impregnated with pyrethroids constitute a major tool for malaria control in this region. Efficacy of this tool can be hampered by resistance to the pyrethroids in the Anopheles mosquito vectors. Resistance status of these mosquitoes in this region is poorly understood, effectively hampering better understanding of the impact of LLINs in the malaria control initiative. Here, we assessed susceptibility of the Anopheles arabiensis from the region to deltamethrin, permethrin (pyrethroids) and pirirmiphos-methyl (organophosphate) insecticides. Method: We collected anopheline mosquito larvae from their natural habitats and reared them to adult emergence in situ field insectary in Karamoja region. We then identified them morphological to species level and exposed 513 emerge adult female An gambiae s.l., mosquitoes to diagnostic dosages of deltamethrin (0.05%), permethrin (0.75%) and pirimiphos-methyl (0.25%) pyrethroids exposure using the standard WHO insecticide susceptibility test assay. Synergic assays using piperonyl butoxide (PBO) were done to check for the involvement of detoxification enzymes in pyrethroid resistant populations. We then screened for knockdown resistance (KDR) and mosquito species diversity using Polymerase Chain Reaction (PCR). Results: Majority (96%) of the mosquitoes we sampled were identified as An. arabiensis and 4% as An. gambiae sensu stricto. We observed cross-resistance to both deltamethrin (11.9%) and permethrin (47%) but susceptibility (100% mortality) to pirimiphos-methyl in An. arabiensis. The pre-exposure to PBO ameliorated the resistance to both pyrethroids. We detected homozygous KDR -eastern variant in 1.8 and 50% of the An. arabiensis and An. gambiae s.s. respectively. Conclusion: Anopheles arabiensis and An. gambiae s.s. are the malaria vector in Karamoja region with An. arabiensis predominating. Both species are susceptible to pirimiphos-methyl but resistant to both deltamethrin and permethrin, through a metabolic process (phenotype). Mosquotoes with genetic (kdr) mutations for resistance were minimal and hence have minimal contribution to the pyrethroid resistance profile. An. arabiensis can thus be controled in Karamoja region using deltamethrin and/or permethrin impregnated mosquito nets integrated with PBO and/or through indoor residual spraying of sprayable human dwellings with pirimiphos-methyl.Item 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, AdalgisaUnderstanding 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.Item Spatial Distribution of Tsetse Flies and Trypanosome Infection Status in a Vector Genetic Transition Zone in Northern Uganda(Journal of Parasitology Research, 2022) Opiro, Robert; Okello Allele, Moses,; Opoke, Robert; Oloya, Francis A.; Nakafu, Esther; Iwiru, Teresa; Echodu, Richard; Malinga, Geoffrey M.; Bargul, Joel L.; Opiyo, Elizabeth A.Tsetse flies are vectors of the genus Trypanosoma that cause African trypanosomiasis, a serious parasitic disease of people and animals. Reliable data on the vector distribution and the trypanosome species they carry is pertinent for planning sustainable control strategies. This study was carried out to estimate the spatial distribution, apparent density, and trypanosome infection rates of tsetse flies in two districts that fall within a vector genetic transition zone in northern Uganda. Materials and Methods. Capturing of tsetse flies was done using biconical traps deployed in eight villages in Oyam and Otuke, two districts that fall within the vector genetic transition zone in northern Uganda. Trapped tsetse flies were sexed and morphologically identified to species level and subsequently analyzed for detection of trypanosome DNA. Trypanosome DNA was detected using a nested PCR protocol based on primers amplifying the internal transcribed spacer (ITS) region of ribosomal DNA. Results. A total of 717 flies (406 females; 311 males) were caught, all belonging to the Glossina fuscipes fuscipes species. The overall average flies/trap/day (FTD) was 2:20 ± 0:3527 (mean ± SE). Out of the 477 (201 male; 276 females) flies analyzed, 7.13% (34/477) were positive for one or more trypanosome species. Three species of bovine trypanosomes were detected, namely, Trypanosoma vivax, 61.76% (21/34), T. congolense, 26.47% (9/34), and T. brucei brucei, 5.88% (2/34), and two cases of mixed infection of T. congolense and T. brucei brucei, 5.88% (2/34). The infection rate was not significantly associated with the sex of the fly (generalized linear model (GLM), χ2 = 0:051, p = 0:821, df = 1, n = 477) and district of origin (χ2 = 0:611, p = 0:434, df = 1, n = 477). However, trypanosome infection was highly significantly associated with the fly’s age based on wing fray category (χ2 = 7:56, p = 0:006, df = 1, n = 477), being higher among the very old than the young. Conclusion. The relatively high tsetse density and trypanosome infection rate indicate that the transition zone is a highrisk area for perpetuating animal trypanosomiasis. Therefore, appropriate mitigation measures should be instituted targeting tsetse and other biting flies that may play a role as disease vectors, given the predominance of T. vivax in the tsetse samples.Item 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, AdalgisaTsetse 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.