How does host age and nutrition affect density regulation of obligate versus facultative bacterial symbionts? Insights from the tsetse fly

Abstract

The relationships between insect hosts and their symbionts can vary tremendously in the extent to which hosts depend on and control their symbionts. Obligate symbionts that provide micronutrients to their host are often compartmentalised to specialised host organs and depend on their hosts for survival, whereas facultative symbionts retain the ability to survive outside of their hosts. Few studies compare the extent to which a host controls and adjusts the density of obligate and facultative symbionts directly. Here, we used tsetse as a model for teasing apart the relationships between a host (Glossina morsitans morsitans) and obligate (Wigglesworthia glossinidia) and facultative (Sodalis glossinidius) symbionts. We hypothesised that tsetse actively regulate the density of Wigglesworthia according to the hosts requirements, depending on their current nutritional state and developmental age. In contrast, we postulated that Sodalis retains some independence from host control, and that the growth of this symbiont is dependent on the conditions of the immediate environment, such as nutrient availability. Using qPCR, we examined how symbiont densities change across host age and the hunger cycle. Additionally, we investigated how host nutrition influences symbiont density, by comparing tsetse that were fed diluted blood (poor nutrition) or blood supplemented with yeast extract (vitamin enriched). We found that the density of Wigglesworthia did not reflect the nutritional status of the host, but was optimised to accommodate long-term host requirements (in terms of nutrient provisioning). In contrast, the density of facultative Sodalis was influenced by the ecological context (i.e. nutrient availability). This suggests that tsetse regulate the abundance of Wigglesworthia to a greater extent than Sodalis. We propose that tsetse exert only partial control over Sodalis growth due to the relatively recent transition of this symbiont to host-associated living. Author summarySymbiotic microbes have the potential to significantly impact the wider ecosystem by affecting the fitness and behaviour of their animal hosts. The density of a particular symbiont population within host tissues is likely an important factor influencing the effect it has on the host, however, little is known about the factors which determine how symbiont density is regulated, and how these differ between symbionts with different degrees of host-association (e.g. obligate and facultative symbionts). Here, we found that Wigglesworthia and Sodalis, two bacterial tsetse symbionts, demonstrate distinct trends in density according to host age and nutrition. We discuss how the evolutionary histories of these symbionts with their host potentially explain these results, highlighting the complexity and dynamic nature of host-symbiont interactions. Our findings contribute to our understanding of the extent to which hosts and symbionts control symbiont density and how symbiont density regulation can be affected by the ecological context.