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Echodu, R.

Publications and source records attributed to Echodu, R..

4 recordsLinked to original sources

Mapping tsetse fly connectivity in Uganda with machine learning landscape genetics

Introduction - Tsetse flies (genus Glossina) are biting insects that transmit human and animal trypanosomiases across sub-Saharan Africa, and sustainable vector control depends on understanding dispersal barriers and reinvasion routes. Despite major progress toward elimination, Uganda remains at risk for both human forms of the disease (Trypanosoma brucei gambiense and T. b. rhodesiense) and planners still lack reliable maps of tsetse movement and reinvasion risk. Methods and Results - We address this gap with machine-learning landscape genetics and species distribution models, integrating estimates of population genetic distance and geospatial environmental data to predict and map Glossina fuscipes fuscipes connectivity across Uganda and western Kenya. Inputs included microsatellite genotypes from 11 loci genotyped in 2,736 flies sampled from 87 localities and remotely sensed environmental predictors summarized along least-cost paths. Random forest models predicted patterns of genetic differentiation better than distance-only models, supporting the use of a machine-learning framework for connectivity inference across complex heterogeneous landscapes, and identified variables related to temperature and water availability as the strongest predictors of genetic connectivity. Conclusions - Combining landscape genetics predictions of connectivity with a species distribution model revealed regions with high habitat suitability but low connectivity that represent priority zones for area-wide integrated pest management strategies, including established riverine control tools such as tiny targets and other targeted interventions aimed at reducing reinvasion risk. These results provide biologically interpretable maps and quantitative uncertainty metrics that can guide targeted tsetse control, while providing a transferable analytical pipeline for modeling and mapping genetic connectivity across other species and landscapes.

evolutionary biology↗

Endosymbiont hijacking of acylcarnitines regulates insect vector fecundity by suppressing the viability of stored sperm

Competition between insects and their endosymbiotic bacteria for environmentally limited nutrients can compromise the fitness of both organisms. Tsetse flies, the vectors of pathogenic African trypanosomes, harbor a species and population-specific consortium of vertically transmitted endosymbiotic bacteria that range on the functional spectrum from mutualistic to parasitic. Tsetses indigenous microbiota can include a member of the genus Spiroplasma, and infection with this bacterium causes fecundity-reducing phenotypes in the fly that include a prolonged gonotrophic cycle and a reduction in the motility of stored spermatozoa post-copulation. Herein we demonstrate that Spiroplasma and tsetse spermatozoa compete for fly-derived acylcarnitines, which in other bacteria and animals are used to maintain cell membranes and produce energy. The fat body of mated female flies increases acylcarnitine production in response to infection with Spiroplasma. Additionally, their spermathecae (sperm storage organs), and likely the sperm within, up-regulate expression of carnitine O-palmitoyltransferase-1, which is indicative of increased acylcarnitine metabolism and thus increased energy demand and energy production in this organ. These compensatory measures are insufficient to rescue the motility defect of spermatozoa stored in the spermathecae of Spiroplasma-infected females and thus results in reduced fly fecundity. Tsetses taxonomically simple and highly tractable indigenous microbiota make the fly an efficient model system for studying the biological processes that facilitate the maintenance of bacterial endosymbioses, and how these relationships impact conserved mechanisms (mammalian spermatozoa also use acylcarnitines as an energy source) that regulated animal host fecundity. In the case of insect pests and vectors, a better understanding of the metabolic mechanisms that underlie these associations can lead to the development of novel control strategies. Author SummaryAnimals and the endosymbiotic bacteria that live inside them often compete for nutrients that both organisms require in order to survive. Tsetse flies, which transmit pathogenic African trypanosomes, can house several endosymbionts that have different impacts on their hosts physiological well-being. Female tsetse flies that are infected with one of these bacteria, Spiroplasma, produce fewer offspring than do their uninfected counterparts. In this study we demonstrate that the bacterium and the flys sperm cells (spermatozoa) compete for a specific type of lipid called acylcarnitines. When mated female tsetse flies are experimentally manipulated to produce less acylcarnitine Spiroplasma density decreases. Additionally, spermatozoa stored in the sperm storage organs of acylcarnitine depleted females lose motility and are eventually resorbed, thus rendering the females reproductively sterile. These findings mechanistically demonstrate how endosymbiotic bacteria can manipulate their hosts reproductive potential. In the case of arthropods that transmit pathogenic microbes, this relationship has significant implications for disease transmission and epidemiology.

microbiology↗

Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis

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 hosts 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 flys resistance to infection with trypanosomes. However, the potential impact of Spiroplasma on tsetses 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 tsetses reproductive fitness. Using a Gff 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. Author SummaryEndosymbiotic bacteria regulate numerous aspects of their hosts reproductive physiology. Natural populations of the tsetse fly, Glossina fuscipes fuscipes (Gff), house heterogeneous infections with the bacterium Spiroplasma glossinidia. Infection with the bacterium results in the presentation of several phenotypes in both male and female Gff that would put them at a significant reproductive disadvantage when compared to their counterparts that do not house the bacterium. These Spiroplasma induced phenotypes include changes in sex-biased gene expression in the reproductive organs, a depletion in the availability of metabolically critical lipids in pregnant females that results in delayed larval development, and compromised sperm fitness. These findings indicate that Spiroplasma exerts an overall negative impact on both male and female reproductive fitness and thus likely has a profound effect on fly population structure. This outcome, in conjunction with the fact that Spiroplasma infected tsetse are unusually refractory to infection with pathogenic African trypanosomes, indicates that the bacterium could be experimentally exploited to reduce disease transmission through the fly.

microbiology↗

Spatio-temporal distribution of Spiroplasma infections in the tsetse fly (Glossina fuscipes fuscipes) in northern Uganda

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 hosts 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.\n\nGeneralized 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.\n\nAuthor SummaryWe investigated the association of symbiotic Spiroplasma with the tsetse fly host Glossina fuscipes fuscipes (Gff) to assess if Spiroplasma infections are correlated with Gff genetic background, geography, or season and its interaction with trypanosome parasites. We analyzed distribution and prevalence of Spiroplasma infections across different Gff sampling sites in northern and western Uganda, and found that the symbiont is unevenly distributed and infections have not reached fixation within these sampling sites. We tested for associations with geographic origin of the collections, seasonal environmental conditions at the time of collection, Gff host genetic background and sex, plus trypanosome co-infections. Spiroplasma prevalence was strongly correlated with geographic origin and seasonal environmental conditions. Our parasite infection data suggested a negative correlation of Spiroplasma with trypanosome infection, with only 5 out of 243 flies harboring trypanosome co-infections. We further investigated the influence of Spiroplasma on trypanosome parasite infections in the laboratory. We found that trypanosomes were less likely to establish an infection in Gff individuals that carried Spiroplasma infections. Our results provide new information on host-endosymbiont dynamics in an important human disease vector, and provide evidence that Spiroplasma may confer partial resistance to Gff trypanosome infections. These findings provide preliminary evidence that a symbiont-based control method could be successful in combating tsetse trypanosome transmission to humans and livestock in sub-Saharan Africa.

epidemiology↗