Mechanisms and Evolution of Heritable Microbial Density in Insect Hosts

Parker, Benjamin J.

doi:10.1128/msystems.00728-21

Cited by 7 publications

(6 citation statements)

References 25 publications

(39 reference statements)

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“…It would be interesting to explore the paternal transmission process and horizontal transmission routes of facultative symbionts (e.g., Rickettsia ) in cicadas, which may provide new information about the transmission strategies of symbionts in cicadas and other auchenorrhynchan insects. Manipulation of symbiotic organs or microbial symbiont(s) seems to be a novel strategy for the control of insect pests especially for plant sap-feeding insects [ 48 – 50 ]. Studies on the diversification and transovarial transmission of symbionts in cicadas provide not only novel insights into uncovering complicated host-symbiont associations but also helpful guidelines for the control of sap-feeding pests.…”

Section: Discussionmentioning

confidence: 99%

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

Huang,

Wang,

Zhou

et al. 2024

Front Zool

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The most extraordinary systems of symbiosis in insects are found in the suborder Auchenorrhyncha of Hemiptera, which provide unique perspectives for uncovering complicated insect-microbe symbiosis. We investigated symbionts associated with bacteriomes and fat bodies in six cicada species, and compared transmitted cell number ratio of related symbionts in ovaries among species. We reveal that Sulcia and Hodgkinia or a yeast-like fungal symbiont (YLS) are segregated from other host tissues by the bacteriomes in the nymphal stage, then some of them may migrate to other organs (i.e., fat bodies and ovaries) during host development. Particularly, YLS resides together with Sulcia in the “symbiont ball” of each egg and the bacteriomes of young-instar nymphs, but finally migrates to the fat bodies of adults in the majority of Hodgkinia-free cicadas, whereas it resides in both bacteriome sheath and fat bodies of adults in a few other species. The transmitted Sulcia/YLS or Sulcia/Hodgkinia cell number ratio in ovaries varies significantly among species, which could be related to the distribution and/or lineage splitting of symbiont(s). Rickettsia localizes to the nuclei of bacteriomes and fat bodies in some species, but it was not observed to be transmitted to the ovaries, indicating that this symbiont may be acquired from environments or from father to offspring. The considerable difference in the transovarial transmission process of symbionts suggests that cellular mechanisms underlying the symbiont transmission are complex. Our results may provide novel insights into insect-microbe symbiosis.

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Section: Discussionmentioning

confidence: 99%

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

Huang,

Wang,

Zhou

et al. 2024

Front Zool

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“…A recent experimental evolution study of Wolbachia infections in Drosophila , for example, did not find any reduction of symbiont density or in the fitness costs of symbionts to hosts across 17 generations of lab conditions expected to select for reduced symbiont virulence (40). The authors speculate that within-host pressures select for symbionts with higher density despite the increased cost to hosts (5, 40, 41). Together these studies suggest that vertically-transmitted symbionts are subject to the same tradeoffs between virulence and transmission that shape pathogen coevolutionary dynamics, and stress the critical importance of within-host dynamics in the evolution of vertically-transmitted symbioses.…”

Section: Discussionmentioning

confidence: 99%

“…These symbiotic associations can range from parasitic to mutualistic, and symbionts have been shown to influence host traits including host plant use, body color, and defense against natural enemies (2,3). An important aspect of insect-symbiont interactions is the within-host density of symbiont infections (4)(5)(6). Symbiont density has been shown to vary across individual insects, driven in part by genetic variation among microbes and/or hosts (7).…”

Section: Introductionmentioning

confidence: 99%

Variation in density, immune gene suppression, and co-infection outcomes among strains of the aphid endosymbiont Regiella insecticola

Goldstein

Acosta

Henry

et al. 2022

Preprint

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Many insects harbor heritable beneficial microbes that influence host phenotypes. Across systems, divergent symbiont strains have been shown to establish at different densities within hosts. This genetic variation is important evolutionarily because within-host density has been linked to the costs and benefits of the symbiosis for both partners. Studying the factors shaping within-host density is therefore important to our broader understanding of host-microbe coevolution. Here we focused on different strains of Regiella insecticola, a facultative symbiont of aphids. We first demonstrated that different strains of Regiella consistently establish in pea aphids at drastically different densities. We then found that variation in density is correlated with the expression levels of two key insect immune system genes (phenoloxidase and hemocytin), with immune gene suppression correlating with higher Regiella density. We then performed an experiment where we established co-infections of a higher- and lower-density Regiella strain, and we showed that the higher-density strain is better able to persist in co-infections than the lower-density strain. Together, our results point to a potential mechanism for strain-level variation in symbiont density in this system, and further suggest that symbiont fitness may be increased by establishing at higher density within hosts. Our work highlights the importance of within-host dynamics shaping symbiont evolution.

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“…Based on genomic predictions, facultative endosymbionts appear be generally auxotrophic for several essential resources, in particular amino acids, and rely on their insect host to sustain their metabolism (Degnan et al, 2009;Renoz et al, 2021). Negative correlations between host fitness traits and facultative endosymbiont densities observed in aphids and Drosophila tend to support the hypothesis of energetic demand imposed by the symbionts that further depress their host fitness (Cayetano et al, 2015;Leclair et al, 2017;Parker, 2021;Weldon et al, 2013). Second, in facultative associations, hosts present generally heightened immune-related functions to control bacterial density (Laughton et al, 2014).…”

Section: Introductionmentioning

confidence: 96%

Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

et al. 2022

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1. Many insect species harbour heritable bacterial endosymbionts. Some facultative endosymbionts provide benefits to their hosts under certain environmental conditions.2. Facultative endosymbionts are expected to impose additional energetic expenditures to their host, reducing host fitness. While there is accumulating evidence in plant sucking insects that facultative endosymbionts reduce the fitness of their host under permissive conditions, no direct energy costs associated with facultative endosymbionts have been identified.3. Using the standard metabolic rate (SMR) as a measure of the energy cost of selfmaintenance, we investigated whether two common facultative endosymbionts Hamiltonella defensa or Regiella insecticola increase the maintenance cost of the pea aphid Acyrthosiphon pisum which could translate into host fitness reduction ('compensation hypothesis'). In addition, we tested if there was a link between SMR and the aphid fitness and whether it depended on endosymbiont density and aphid energetic reserves. Finally, we measured SMR at different temperatures to assess the impact of suboptimal thermal conditions on physiological cost of endosymbionts.4. In the presence of facultative endosymbionts, aphids expressed generally a lower fitness and a higher SMR compared to uninfected ones, in accordance with the 'compensation hypothesis'. However, the SMR difference between infected and uninfected aphids tended to decrease with increasing temperature. Complex host genotype-by-symbiont genotype-by-temperature interactions on SMR were also revealed.5. Energetic budget of adult aphids appeared weakly influenced by the aphid genotype and endosymbiont species, suggesting that facultative endosymbionts primarily impact the consumption of energy resources rather than their acquisition. Density of facultative endosymbionts varied largely among aphid lines but was not associated with the fitness nor metabolic rate of aphids.

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Mechanisms and Evolution of Heritable Microbial Density in Insect Hosts

Abstract: Within-host density is a critically important aspect of vertically transmitted symbioses that influences the fitness of both hosts and microbes. I review recent studies of symbiont density in insects, including my laboratory’s work on pea aphids and maternally transmitted bacteria.

Cited by 7 publications

References 25 publications

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

Segregation of endosymbionts in complex symbiotic system of cicadas providing novel insights into microbial symbioses and evolutionary dynamics of symbiotic organs in sap-feeding insects

Variation in density, immune gene suppression, and co-infection outcomes among strains of the aphid endosymbiont Regiella insecticola

Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

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