Sodalis glossinidius presence in wild tsetse is only associated with presence of trypanosomes in complex interactions with other tsetse-specific factors

Abstract

BackgroundSusceptibility of tsetse flies (Glossina spp.) to trypanosomes of both humans and animals has been associated with the presence of the endosymbiont Sodalis glossinidius. However, intrinsic biological characteristics of the flies and environmental factors can influence the presence of both S. glossinidius and the parasites. It thus remains unclear whether it is the S. glossinidius or other attributes of the flies that explains the apparent association. The objective of this study was to test whether the presence of Trypanosoma vivax, T. congolense and T. brucei are related to the presence of S. glossinidius in tsetse flies when other factors are accounted for: geographic location, species of Glossina, sex or age of the host flies.ResultsFlies (n = 1090) were trapped from four sites in the Shimba Hills and Nguruman regions in Kenya. Sex and species of tsetse (G. austeni, G. brevipalpis, G. longipennis and G. pallidipes) were determined based on external morphological characters and age was estimated by a wing fray score method. The presence of trypanosomes and S. glossinidius was detected using PCR targeting the internal transcribed spacer region 1 and the haemolysin gene, respectively. Sequencing was used to confirm species identification. Generalised Linear Models (GLMs) and Multiple Correspondence Analysis (MCA) were applied to investigate multivariable associations. The overall prevalence of trypanosomes was 42.1%, but GLMs revealed complex patterns of associations: the presence of S. glossinidius was associated with trypanosome presence but only in interactions with other factors and only in some species of trypanosomes. The strongest association was found for T. congolense, and no association was found for T. vivax. The MCA also suggested only a weak association between the presence of trypanosomes and S. glossinidius. Trypanosome-positive status showed strong associations with sex and age while S. glossinidius-positive status showed a strong association with geographic location and species of fly.ConclusionsWe suggest that previous conclusions about the presence of endosymbionts increasing probability of trypanosome presence in tsetse flies may have been confounded by other factors, such as community composition of the tsetse flies and the specific trypanosomes found in different regions.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1285-6) contains supplementary material, which is available to authorized users.

Blood meal analysis of tsetse flies (Glossina pallidipes: Glossinidae) reveals higher host fidelity on wild compared with domestic hosts

“…The G. pallidipes samples used in this study for host blood meal analysis were the same as those described in Channumsin et al (2018), where details of the sampling strategy are provided (but see Supplementary Table 1 for locations of the traps). Tsetse flies were collected from three sites that differ in anticipated levels of abundance of livestock and wildlife.…”

“…Characteristics of the flies and presence of trypanosomes were taken from Channumsin et al (2018). Whole flies were preserved in 95% ethanol and stored at - 80°C.…”

“…2005)) that allow identification of trypanosome species based on size of amplicons. For blood meal analyses in this study, we used DNA extracted from abdomen samples from the G. pallidipes (N = 577) samples described in Channumsin et al (2018).…”

“…Model selection was performed using likelihood ratio tests to find the minimum model that best explained the data. The same approach was used to test whether the presence of trypanosomes was explained by feeding behaviour, host type, site, or tsetse-specific factors, including all pairwise interactions and a three-way interaction between sex, age and site, based on conclusions from the previous study (Channumsin et al . 2018).…”

“…In a previous study, we established that the prevalence of trypanosomes in two regions of Kenya (Nguruman and the Shimba Hills) showed complex relationships with geographic location, tsetse specific factors (age, sex and fly species), species of trypanosome and the presence of an endosymbiont, Sodalis glossinidius (Channumsin et al . 2018).…”