Heritability of symbiont density reveals distinct regulatory mechanisms in a tripartite symbiosis

Abstract

Beneficial eukaryotic–bacterial partnerships are integral to animal and plant evolution. Understanding the density regulation mechanisms behind bacterial symbiosis is essential to elucidating the functional balance between hosts and symbionts. Citrus mealybugs, Planococcus citri (Risso), present an excellent model system for investigating the mechanisms of symbiont density regulation. They contain two obligate nutritional symbionts, Moranella endobia, which resides inside Tremblaya princeps, which has been maternally transmitted for 100–200 million years. We investigate whether host genotype may influence symbiont density by crossing mealybugs from two inbred laboratory‐reared populations that differ substantially in their symbiont density to create hybrids. The density of the M. endobia symbiont in the hybrid hosts matched that of the maternal parent population, in keeping with density being determined either by the symbiont or the maternal genotype. However, the density of the T. princeps symbiont was influenced by the paternal host genotype. The greater dependency of T. princeps on its host may be due to its highly reduced genome. The decoupling of T. princeps and M. endobia densities, in spite of their intimate association, suggests that distinct regulatory mechanisms can be at work in symbiotic partnerships, even when they are obligate and mutualistic.

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

“…However, a study of B. aphidicola in A. pisum reports that the obligate symbiont titre varies among host clones, indicating that host genotype is an influential factor in infection density (Vogel & Moran, ). In addition, sexual hybridization experiments between citrus mealybug and A. pisum populations both indicate a link between host genotype and symbiont density (Vogel & Moran, ; Parkinson et al ., ). Given the diversity of bacterial symbiotic associations in insects, caution should be taken when comparing the results from studies involving different species.…”

“…To determine whether the intensities of M. endobia and T. princeps infections differed between mealybug populations, we used a quantitative polymerase chain reaction (PCR) with symbiont‐specific primers and protocols to quantify symbiont versus host genome copy number in replicate mealybugs from each population (see below) (Parkinson et al ., , ). It should be noted that symbiont genome copy number can only be used as a proxy for symbiont density because of the polyploid nature of insect symbionts and bacteriocytes; thus, the actual number of symbiont cells may be much lower (von Dohlen et al ., ; Baumann, ; Downie & Gullan, ).…”

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…Phylogenetic analyses of the intra-Tremblaya endosymbionts show that, although different lineages of mealybugs in the Pseudococcinae all possess γ-proteobacterial endosymbionts related to Sodalis, these bacteria do not show the coevolutionary patterns typical of many long-term endosymbionts (43,44,46). Developmental studies suggest that Tremblaya and its resident γ-proteobacteria can be differentially regulated by the host (44,47). These data raise the possibility that the innermost bacterium of this symbiosis is labile and may have resulted from separate acquisitions, or that the original intra-Tremblaya symbiont has been replaced in different mealybug lineages.…”

Phylogenetic analyses and characteristics of the microbiomes from five mealybugs (Hemiptera: Pseudococcidae)

“…As a result, we concluded that certain groups within the microbiota and the bacterial richness in the insect gut may be affected by the host diet, habitat, and developmental stage (Yun et al, ). Certainly, the diversity of plant nutrient sources may also affect the abundance of bacteria in the host insects that feed on plants (Francis & Currie, ; Parkinson, Gobin, & Hughes, ).…”

“…Certainly, the diversity of plant nutrient sources may also affect the abundance of bacteria in the host insects that feed on plants (Francis & Currie, 2003;Parkinson, Gobin, & Hughes, 2016).…”