Browsing by Author "Saarman, Norah P."

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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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    Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis
    (PLoS pathogens, 2021) Son, Jae Hak; Weiss, Brian L.; Schneider, Daniela I.; Dera, Kiswend-sida M.; Gstottenmayer, Fabian; Opiro, Robert; Echodu, Richard; Saarman, Norah P.; Attardo, Geoffrey M.; Onyango, Maria; Abd-Alla, Adly M. M.; Aksoy, Serap
    Tsetse flies (Glossina spp.) house a population-dependent assortment of microorganisms that can include pathogenic African trypanosomes and maternally transmitted endosymbiotic bacteria, the latter of which mediate numerous aspects of their host’s metabolic, reproductive, and immune physiologies. One of these endosymbionts, Spiroplasma, was recently discovered to reside within multiple tissues of field captured and laboratory colonized tsetse flies grouped in the Palpalis subgenera. In various arthropods, Spiroplasma induces reproductive abnormalities and pathogen protective phenotypes. In tsetse, Spiroplasma infections also induce a protective phenotype by enhancing the fly’s resistance to infection with trypanosomes. However, the potential impact of Spiroplasma on tsetse’s viviparous reproductive physiology remains unknown. Herein we employed high-throughput RNA sequencing and laboratory-based functional assays to better characterize the association between Spiroplasma and the metabolic and reproductive physiologies of G. fuscipes fuscipes (Gff), a prominent vector of human disease. Using field-captured Gff, we discovered that Spiroplasma infection induces changes of sex-biased gene expression in reproductive tissues that may be critical for tsetse’s reproductive fitness. Using a Gff lab line composed of individuals heterogeneously infected with Spiroplasma, we observed that the bacterium and tsetse host compete for finite nutrients, which negatively impact female fecundity by increasing the length of intrauterine larval development. Additionally, we found that when males are infected with Spiroplasma, the motility of their sperm is compromised following transfer to the female spermatheca. As such, Spiroplasma infections appear to adversely impact male reproductive fitness by decreasing the competitiveness of their sperm. Finally, we determined that the bacterium is maternally transmitted to intrauterine larva at a high frequency, while paternal transmission was also noted in a small number of matings. Taken together, our findings indicate that Spiroplasma exerts a negative impact on tsetse fecundity, an outcome that could be exploited for reducing tsetse population size and thus disease transmission.
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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.