Abstract
Many insects rely on intracellular bacterial symbionts to supplement their specialized diets with micronutrients. Using data from diverse and well-studied insect systems, we propose three lines of evidence suggesting that hosts have tight control over the density of their obligate, intracellular bacterial partners. First, empirical studies have demonstrated that the within-host symbiont density varies depending on the nutritional and developmental requirements of the host. Second, symbiont genomes are highly reduced and have limited capacity for self-replication or transcriptional regulation. Third, several mechanisms exist for hosts to tolerate, regulate and remove symbionts including physical compartmentalization and autophagy. We then consider whether such regulation is adaptive, by discussing the relationship between symbiont density and host fitness. We discuss current limitations of empirical studies for exploring fitness effects in host–symbiont relationships, and emphasize the potential for using mathematical models to formalize evolutionary hypotheses and to generate testable predictions for future work.
Highlights
Beneficial relationships between bacteria and animals are extremely common in nature
A characteristic of many obligate bacterial symbionts of insects is that the symbiont is located intracellularly within the host, in specialized and relatively large cells known as bacteriocytes [8]
The results showed that the different clones have different requirements for dietary essential amino acids (EAAs), and a subsequent study determined that these requirements were moderately and positively correlated with the density of Buchnera found in these hosts [39]
Summary
Beneficial relationships between bacteria and animals are extremely common in nature. From the insect systems reviewed three distinct patterns of intracellular symbiont density dynamics emerge: sustained symbiont proliferation throughout host development (e.g. female tsetse and psyllids); symbiont density increase in early adulthood, followed by a reduction in symbiont density (e.g. male tsetse and aphids); and symbiont density increase in early adulthood, followed by symbiont removal or near-removal (e.g. carpenter ants and cereal weevils) Explanations for these trends have been proposed by considering the benefits and costs of the symbiosis to the host, as well as how the nutritional requirements of the hosts may change throughout development and with respect to reproduction. The results of the experimental studies reviewed support the idea that insects have tight control of their symbiont densities, and that these densities are regulated by the hosts in response to their developmental and nutritional requirements This leads to the central question of whether such symbiont regulation maximizes the net fitness benefit for hosts participating in a symbiosis. The intimacy of the relationship between insects and their obligate intracellular symbionts renders many questions about these symbioses difficult to approach empirically, and applying theoretical methods could help open new avenues for research and inspire interesting new questions
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