Unrelated facultative endosymbionts protect aphids against a fungal pathogen.
TL;DR: It is shown that protection against this entomopathogen, Pandora neoaphidis, can be conferred by strains of four distantly related symbionts (in the genera Regiella,Rickettsia, Rickettsiella and Spiroplasma), which reduce mortality and also decrease fungal sporulation on dead aphids which may help protect nearby genetically identical insects.
Abstract: The importance of microbial facultative endosymbionts to insects is increasingly being recognized, but our understanding of how the fitness effects of infection are distributed across symbiont taxa is limited. In the pea aphid, some of the seven known species of facultative symbionts influence their host's resistance to natural enemies, including parasitoid wasps and a pathogenic fungus. Here we show that protection against this entomopathogen, Pandora neoaphidis, can be conferred by strains of four distantly related symbionts (in the genera Regiella, Rickettsia, Rickettsiella and Spiroplasma). They reduce mortality and also decrease fungal sporulation on dead aphids which may help protect nearby genetically identical insects. Pea aphids thus obtain protection from natural enemies through association with a wider range of microbial associates than has previously been thought. Providing resistance against natural enemies appears to be a particularly common way for facultative endosymbionts to increase in frequency within host populations.
Citations
More filters
TL;DR: It is proposed that balancing selection plays a major role in symbiont maintenance, with protective benefits in the presence of enemies and infection costs in their absence, and knowledge of the functional mechanisms behind protection and natural symbionts dynamics could be key to understanding many of the world's antagonistic species interactions.
Abstract: Summary
Symbiotic microbes have become increasingly recognized to mediate interactions between natural enemies and their hosts. The ecologies of these symbioses, however, are poorly understood in many systems, and a predictive framework is needed to guide future studies. To achieve this, we focus on heritable, defensive microbes of insects. Our review of laboratory-based studies identifies diverse bacterial species that have independently evolved to protect a range of insects against parasitoids, parasites, predators and pathogens. Although defensive mechanisms are typically unknown, some involve toxins or the upregulation of host immunity.
Despite substantial benefits of infection in the presence of natural enemies, the protective symbionts of insects are often found at intermediate levels in natural populations. Using a host-centred population genetics approach made possible by the host restriction and cytoplasmic inheritance of these microbes, we propose that balancing selection plays a major role in symbiont maintenance, with protective benefits in the presence of enemies and infection costs in their absence. Other mediating factors are likely to be important, including temperature, superinfections and transmission dynamics.
While few studies have provided evidence for defence in the field, several studies have shown symbiont infection frequencies to be dynamic, varying across temporal and spatial gradients and food–plant associations. Newly presented data from our pea aphid research reveal that temporal shifts in defensive symbiont prevalence can be quite rapid, with Hamiltonella defensa showing 10–20% shifts around a seasonal average of c. 50%. Such findings contrast with more unidirectional changes seen in laboratory population cages, suggesting temporal changes in the costs and benefits of symbionts in the field.
To frame future research on defensive symbiont ecology, we briefly consider a range of studies needed to test laboratory- and field-derived predictions on defensive symbiosis. Included are investigations of defensive mechanisms, symbiont-driven co-evolution and community-level effects. We also consider the need for more thorough and highly resolved molecular diagnostics of natural infections, laboratory studies on functional differences between symbiont strains and species and studies on the relative costs and benefits of defenders in nature.
The emerging theme of symbiont-mediated defence across eukaryotes suggests that knowledge of the functional mechanisms behind protection and natural symbiont dynamics could be key to understanding many of the world's antagonistic species interactions. Thus, the development of insects as a model for such studies holds promise for these organisms and beyond.
306 citations
TL;DR: The described protective symbioses between animals and bacteria, fungi, and dinoflagellates are reviewed to derive general patterns on the chemistry, ecology, and evolution of such associations.
282 citations
TL;DR: It is found that not only is horizontal transfer common, but it is also associated with aphid lineages colonizing new ecological niches, including novel plant species and climatic regions, suggesting significant involvement of symbionts in their host's adaptation to different niches.
231 citations
Cites background from "Unrelated facultative endosymbionts..."
...While not essential for host survival, they often provide significant fitness benefits [1-5]....
[...]
...insecticola are known to confer resistance to different natural enemies [2-4], and were the selective pressures from these organisms to be host-plant specific, it may explain the associations....
[...]
TL;DR: In this article, the authors quantified the cytoplasmically inherited genetic variation contributed by symbionts within North American pea aphids using denaturing gradient gel electrophoresis (DGGE) and 454 amplicon pyrosequencing of 16S rRNA genes.
Abstract: Heritable genetic variation is required for evolution, and while typically encoded within nuclear and organellar genomes, several groups of invertebrates harbour heritable microbes serving as additional sources of genetic variation. Hailing from the symbiont-rich insect order Hemiptera, pea aphids (Acyrthosiphon pisum) possess several heritable symbionts with roles in host plant utilization, thermotolerance and protection against natural enemies. As pea aphids vary in the numbers and types of harboured symbionts, these bacteria provide heritable and functionally important variation within field populations. In this study, we quantified the cytoplasmically inherited genetic variation contributed by symbionts within North American pea aphids. Through the use of Denaturing Gradient Gel Electrophoresis (DGGE) and 454 amplicon pyrosequencing of 16S rRNA genes, we explored the diversity of bacteria harboured by pea aphids from five populations, spanning three locations and three host plants. We also characterized strain variation by analysing 16S rRNA, housekeeping and symbiont-associated bacteriophage genes. Our results identified eight species of facultative symbionts, which often varied in frequency between locations and host plants. We detected 28 cytoplasmic genotypes across 318 surveyed aphids, considering only the various combinations of secondary symbiont species infecting single hosts. Yet the detection of multiple Regiella insecticola, Hamiltonella defensa and Rickettsia strains, and diverse bacteriophage genotypes from H. defensa, suggest even greater diversity. Combined, these findings reveal that heritable bacteria contribute substantially to genetic variation in A. pisum. Given the costs and benefits of these symbionts, it is likely that fluctuating selective forces play a role in the maintenance of this diversity.
182 citations
Cites background from "Unrelated facultative endosymbionts..."
...…wasps; Regiella insecticola, Rickettsia, Rickettsiella and some strains of Spiroplasma protect against fungal pathogens (Scarborough et al. 2005; Łukasik et al. 2012); Serratia symbiotica and Rickettsia (and possibly H. defensa (Russell & Moran 2006)) provide protection against the damaging…...
[...]
...More generally, strains of protective symbionts could vary in the strength of protection conferred against particular genotypes of natural enemies (or even different species of enemy) (Łukasik et al. 2012; Schmid © 2013 Blackwell Publishing Ltd et al. 2012)....
[...]
...When we consider prior findings of protective roles for each of these symbionts (Oliver et al. 2003; Scarborough et al. 2005; Guay et al. 2009; Łukasik et al. 2012), pea aphids potentially employ a diverse repertoire of microbially mediated defensive strategies in the field....
[...]
TL;DR: Several aspects of plant defense are detailed and the interaction of plants and phloem-feeding insects are discussed, including the presence of specific enzymes/effectors in this saliva that is thought to interfere with plant defense responses.
Abstract: Due to the high content of nutrient, sieve tubes are a primary target for pests, e.g., most phytophagous hemipteran. To protect the integrity of the sieve tubes as well as their content, plants possess diverse chemical and physical defense mechanisms. The latter mechanisms are important because they can potentially interfere with the food source accession of phloem-feeding insects. Physical defense mechanisms are based on callose as well as on proteins and often plug the sieve tube. Insects that feed from sieve tubes are potentially able to overwhelm these defense mechanisms using their saliva. Gel saliva forms a sheath in the apoplast around the stylet and is suggested to seal the stylet penetration site in the cell plasma membrane. In addition, watery saliva is secreted into penetrated cells including sieve elements; the presence of specific enzymes/effectors in this saliva is thought to interfere with plant defense responses. Here we detail several aspects of plant defense and discuss the interaction of plants and phloem-feeding insects. Recent agro-biotechnological phloem-located aphid control strategies are presented.
170 citations
Cites background from "Unrelated facultative endosymbionts..."
...Potential candidates for PIMP production are cell-wall-degrading enzymes, such as cellulase and pectinase, which were detected in aphid saliva (Ma et al., 1990; Cherqui and Tjallingii, 2000)....
[...]
References
More filters
Journal Article•
TL;DR: Copyright (©) 1999–2012 R Foundation for Statistical Computing; permission is granted to make and distribute verbatim copies of this manual provided the copyright notice and permission notice are preserved on all copies.
Abstract: Copyright (©) 1999–2012 R Foundation for Statistical Computing. Permission is granted to make and distribute verbatim copies of this manual provided the copyright notice and this permission notice are preserved on all copies. Permission is granted to copy and distribute modified versions of this manual under the conditions for verbatim copying, provided that the entire resulting derived work is distributed under the terms of a permission notice identical to this one. Permission is granted to copy and distribute translations of this manual into another language, under the above conditions for modified versions, except that this permission notice may be stated in a translation approved by the R Core Team.
272,030 citations
"Unrelated facultative endosymbionts..." refers methods in this paper
...The proportion of aphids dying, and of dead sporulating aphids, after exposure to the fungus were analyzed with the statistical package R v. 2.13.0 (R Development Core Team 2011) using logistic generalized linear modelling....
[...]
TL;DR: Insect heritable symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
Abstract: Insect heritable symbionts have proven to be ubiquitous, based on molecular screening of various insect lineages. Recently, molecular and experimental approaches have yielded an immensely richer understanding of their diverse biological roles, resulting in a burgeoning research literature. Increasingly, commonalities and intermediates are being discovered between categories of symbionts once considered distinct: obligate mutualists that provision nutrients, facultative mutualists that provide protection against enemies or stress, and symbionts such as Wolbachia that manipulate reproductive systems. Among the most farreaching impacts of widespread heritable symbiosis is that it may promote speciation by increasing reproductive and ecological isolation of host populations, and it effectively provides a means for transfer of genetic information among host lineages. In addition, insect symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
1,438 citations
"Unrelated facultative endosymbionts..." refers background in this paper
...But it is only more recently that the varied effects that facultative endosymbionts may have on their hosts, which range from pathogenicity through commensalism to true mutualism, have been appreciated (Moran et al. 2008; Ferrari & Vavre 2011)....
[...]
...But it is only more recently that the varied effects that facultative endosymbionts may have on their hosts, which range from pathogenicity through commensalism to true mutualism, have been appreciated (Moran et al. 2008; Ferrari & Vavre 2011)....
[...]
...Facultative endosymbioses are particularly common and involve a broad range of eubacterial taxa (Moran et al. 2008)....
[...]
TL;DR: It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
Abstract: Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
1,235 citations
"Unrelated facultative endosymbionts..." refers background in this paper
...This is in addition to the obligate endosymbiont Buchnera, which provides nutrients missing in phloem sap and is thus essential for aphid survival and found in all individuals (Douglas 1998)....
[...]
TL;DR: Investigation of aphids for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi, shows that infection confers resistance to parasitoids attack by causing high mortality of developing Parasitoid larvae.
Abstract: Symbiotic relationships between animals and microorganisms are common in nature, yet the factors controlling the abundance and distributions of symbionts are mostly unknown. Aphids have an obligate association with the bacterium Buchnera aphidicola (the primary symbiont) that has been shown to contribute directly to aphid fitness. In addition, aphids sometimes harbor other vertically transmitted bacteria (secondary symbionts), for which few benefits of infection have been previously documented. We carried out experiments to determine the consequences of these facultative symbioses in Acyrthosiphon pisum (the pea aphid) for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi, a major natural enemy in field populations. Our results show that, in a controlled genetic background, infection confers resistance to parasitoid attack by causing high mortality of developing parasitoid larvae. Compared with uninfected controls, experimentally infected aphids were as likely to be attacked by ovipositing parasitoids but less likely to support parasitoid development. This strong interaction between a symbiotic bacterium and a host natural enemy provides a mechanism for the persistence and spread of symbiotic bacteria.
1,154 citations
"Unrelated facultative endosymbionts..." refers background in this paper
...…facultative endosymbionts which can protect pea aphids against a fungal pathogen, three others – the gammaproteobacteria H. defensa, Serratia symbiotica and ‘X-type’ – have all been shown or suggested to confer protection against hymenopterous parasitoids (Oliver et al. 2003; Guay et al. 2009)....
[...]
...In the pea aphid, different facultative endosymbionts increase resistance to parasitoid wasps (Oliver et al. 2003) and a pathogenic fungus (Scarborough et al. 2005) as well as help their hosts withstand heat shock (Montllor et al. 2002; Russell & Moran 2006)....
[...]