The more, the merrier? Obligate symbiont density changes over time under controlled environmental conditions, yet holds no clear fitness consequences

Abstract

Symbiotic bacteria are highly diverse, play an important role in ecology and evolution, and are also of applied relevance because many pest insects rely on them for their success. However, the dynamics and regulation of symbiotic bacteria within hosts is complex and still poorly understood outside of a few model systems. One of the most intriguing symbiotic relationships is the obligate, tripartite nutritional mutualism in sap‐feeding, economically‐destructive mealybugs (Hemiptera: Sternorrhyncha: Pseudococcidae), which involves γ‐proteobacteria hosted within β‐proteobacteria hosted within the mealybugs. The present study examines whether there is population variation in symbiont density (i.e. infection intensity, or titre) in the citrus mealybug Planococcus citri (Risso) and how this impacts host life‐history. Symbiont density is found to differ significantly between populations when reared under controlled environmental conditions, indicating that the density of symbiont infections is influenced by host or symbiont genotype. However, symbiont density changes in populations over multiple generations, indicating that symbiont densities are dynamic. Surprisingly, given that the symbionts are essential nutritional mutualists, the density of the symbionts does not correlate significantly with either host fecundity or development. Higher levels of symbionts have no clear benefit to hosts and therefore appear to be superfluous, at least under constant, optimized environmental conditions. Excessive symbiont density may be an evolutionary artefact from a period of inefficient vertical transmission when the balance of conflict between host and symbiont was still being established.

Bacterial communities in natural versus pesticide‐treated Aphis gossypii populations in North China

“…The density of the primary symbiont, Buchnera , in pea aphids tends to decrease with host age and increase with rearing temperature (Lu, Chiu, & Kuo, ). In this study, bacterial density variation was prospected in the natural adult A. gossypii population; the results showed the flexible dynamics of bacterial density over time, although the higher levels of symbionts have no clear benefit to the hosts and therefore appeared to be superfluous (Parkinson et al., ).…”

“…Environmental factors influenced the symbiont density and composition in normal plots, while both were changed depending on the sampled day. Symbiont density is found to differ significantly between the populations when reared under controlled environmental conditions in mealy bugs (Parkinson, Gobin, & Hughes, ). The density of the primary symbiont, Buchnera , in pea aphids tends to decrease with host age and increase with rearing temperature (Lu, Chiu, & Kuo, ).…”

“…although the higher levels of symbionts have no clear benefit to the hosts and therefore appeared to be superfluous (Parkinson et al, 2017).…”

Mutualism or parasitism: Partner abundance affects host fitness in a fish reproductive interaction

“…Because it is so important to host fitness, many hosts have evolved unique strategies to manipulate symbiont or partner abundance to their own advantage (Cunning et al, 2015;Parkinson, Gobin, & Hughes, 2016;Parkinson et al, 2017). For example, crayfish hosts (Cambaridae: Cambarus chasmodactylus and Orconectes cristavarius) actively reduce density of branchiobdellidan worms to prevent a mutualistic cleaning symbiosis from switching to parasitism (Farrell, Creed, & Brown, 2014).…”

Symbionts in excess? No correlation between symbiont density and the ability of mealybug hosts to exploit plant species or tolerate insecticide stress

“…As is the case for aphids and carpenter ants, mealybug obligate symbionts are hypothesized to primarily control gene expression by altering symbiont density within the host (Kono et al ., ). However, a recent study found that laboratory populations of the citrus mealybug under identical environmental conditions differed from each other in their symbiont density, with this density being heritable, although there were no clear fitness benefits or costs associated with higher obligate symbiont density in terms of development, growth or fecundity (Parkinson et al ., , , ).…”