Infections with Immunogenic Trypanosomes Reduce Tsetse Reproductive Fitness: Potential Impact of Different Parasite Strains on Vector Population Structure

Abstract

The parasite Trypanosoma brucei rhodesiense and its insect vector Glossina morsitans morsitans were used to evaluate the effect of parasite clearance (resistance) as well as the cost of midgut infections on tsetse host fitness. Tsetse flies are viviparous and have a low reproductive capacity, giving birth to only 6–8 progeny during their lifetime. Thus, small perturbations to their reproductive fitness can have a major impact on population densities. We measured the fecundity (number of larval progeny deposited) and mortality in parasite-resistant tsetse females and untreated controls and found no differences. There was, however, a typanosome-specific impact on midgut infections. Infections with an immunogenic parasite line that resulted in prolonged activation of the tsetse immune system delayed intrauterine larval development resulting in the production of fewer progeny over the fly's lifetime. In contrast, parasitism with a second line that failed to activate the immune system did not impose a fecundity cost. Coinfections favored the establishment of the immunogenic parasites in the midgut. We show that a decrease in the synthesis of Glossina Milk gland protein (GmmMgp), a major female accessory gland protein associated with larvagenesis, likely contributed to the reproductive lag observed in infected flies. Mathematical analysis of our empirical results indicated that infection with the immunogenic trypanosomes reduced tsetse fecundity by 30% relative to infections with the non-immunogenic strain. We estimate that a moderate infection prevalence of about 26% with immunogenic parasites has the potential to reduce tsetse populations. Potential repercussions for vector population growth, parasite–host coevolution, and disease prevalence are discussed.

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

“…Loss of fecundity could be due to either decreased Wigglesworthia-mediated nutritional effects or to a tradeoff caused by increased host immune activity. A similar loss of fecundity was observed when tsetse were parasitized with trypanosome strains that resulted in host immune induction (22). Thus, these findings further support obligate Wigglesworthia as being indispensible for female fecundity and PGRP-LB as protecting Wigglesworthia from host damage by preventing immune activation.…”

“…The molecular aspects of tsetse's PGRP-LB antitrypanosomal activity remain to be investigated. Because parasite infections and intensity can have a negative impact on host fecundity through immune induction (22), the antiparasitic activity of PGRP-LB can further enhance host fitness.…”

“…Interestingly, silencing PGRP-LB also results in higher susceptibility to trypanosome infections, suggesting a possible antiprotozoal function for PGRP-LB. Given that parasitism induces host immunity, which reduces host fecundity, PGRP-LB can be a strong driver for Wigglesworthia symbiosis and host fitness (22).…”

Vitamin B 6 Generated by Obligate Symbionts Is Critical for Maintaining Proline Homeostasis and Fecundity in Tsetse Flies

“…Parasite infections in various insects result in loss of fecundity rather than reduced longevity (47,48). This outcome is logical since parasite transmission to the next mammalian host depends more upon host vector insect survival and feeding on multiple hosts than upon producing an optimal number of offspring (47)(48)(49).…”

“…This outcome is logical since parasite transmission to the next mammalian host depends more upon host vector insect survival and feeding on multiple hosts than upon producing an optimal number of offspring (47)(48)(49). Tsetse females infected with a highly immunogenic trypanosome strain exhibited decreased fecundity, although these flies lived equally as long as did uninfected tsetse or tsetse infected with a nonimmunogenic parasite strain (47). The decline in fecundity observed in tsetse females infected with the immunogenic parasite strain can be attributed to the physiological cost of host immune system activation (47).…”