Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae

Burke, Gaelen R.; Normark, Benjamin B.; Favret, Colin; Moran, Nancy A.

doi:10.1128/aem.00717-09

Cited by 81 publications

(147 citation statements)

References 39 publications

(68 reference statements)

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“…For example, we speculate that in doubly infected E. inaron the fitness benefit associated with Cardinium may serve to counter the increased metabolic cost of bearing two symbionts, resulting in no net fitness effect for the host. Disentangling such interactive effects among symbionts will become increasingly important as both the frequency of multiple infections (Duron et al, 2008;Burke et al, 2009) Given this dynamism, it seems likely that present-day Cardinium within E. inaron does not have the same functionality as the symbiont that initially invaded the host population. Our study data indicate that neither Cardinium alone nor Cardinium in combination with Wolbachia promotes production of female offspring relative to individuals lacking Cardinium.…”

Section: Discussionmentioning

confidence: 99%

Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium

et al. 2010

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Theory suggests that maternally inherited endosymbionts can promote their spread and persistence in host populations by enhancing the production of daughters by infected hosts, either by improving overall host fitness, or through reproductive manipulation. In the doubly infected parasitoid wasp Encarsia inaron, Wolbachia manipulates host reproduction through cytoplasmic incompatibility (CI), but Cardinium does not. We investigated the fitness costs and/or benefits of infection by each bacterium in differentially cured E. inaron as a potential explanation for persistence of Cardinium in this population. We introgressed lines infected with Wolbachia, Cardinium or both with the cured line to create a similar genetic background, and evaluated several parasitoid fitness parameters. We found that symbiont infection resulted in both fitness costs and benefits for E. inaron. The cost was lower initial egg load for all infected wasps. The benefit was increased survivorship, which in turn increased male production for wasps infected with only Cardinium. Female production was unaffected by symbiont infection; we therefore have not yet identified a causal fitness effect that can explain the persistence of Cardinium in the population. Interestingly, the Cardinium survivorship benefit was not evident when Wolbachia was also present in the host, and the reproduction of doubly infected individuals did not differ significantly from uninfected wasps. Therefore, the results of our study show that even when multiple infections seem to have no effect on a host, there may be a complex interaction of costs and benefits among symbionts.

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Section: Discussionmentioning

confidence: 99%

Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium

et al. 2010

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“…Therefore, Buchnera from different species of aphids may be subspecies, strains or lineages (e.g. Shigenobu et al, 2000;van Ham et al, 2003;Perez-Brocal et al, 2005;Burke et al, 2009, Novákova et al, 2013. According to Ishikawa (2003), the observed diversification of Buchnera indicates that these bacteria can not be considered as representatives of the same species.…”

Section: Discussionmentioning

confidence: 99%

“…The role of secondary endosymbionts is still unclear, but results of recent studies indicate that aphids that possess secondary endosymbionts are more resistant to heat stress (Montlor et al, 2002), attack by parasitic hymenopterans (Oliver et al, 2003;Vorburger et al, 2010) and infection by fungal pathogens (Scarborough et al, 2005) than those that lack them. It is also suggested that secondary endosymbionts may compensate for the loss of the primary endosymbiont of aphids, the bacterium Buchnera (see below) and are able to supplement insufficient provisioning of amino acids usually provided by Buchnera (Koga et al, 2003;Burke et al, 2009). The secondary endosymbionts may be transmitted either vertically or horizontally (Buchner, 1965).…”

Section: Introductionmentioning

confidence: 99%

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Michalik¹,

Szklarzewicz²,

Jankowska³

et al. 2014

Eur. J. Entomol.

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Abstract. The ultrastructure, distribution and transovarial transmission of endosymbiotic bacteria in representatives of six aphid families: Eriosomatidae (Pemphigus spyrothecae, Prociphilus fraxini), Anoeciidae [Anoecia (Anoecia) corni], Drepanosiphidae [Mindarus abietinus, Sipha (Rungsia) maydis, Clethrobius comes, Myzocallis (Lineomyzocallis) walshii], Thelaxidae (Thelaxes dryophila), Aphididae (Delphiniobium junackianum, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria) and Lachnidae (Schizolachnus pineti, Eulachnus rileyi) were studied at the ultrastructural level. The ovaries of aphids are accompanied by large organs termed bacteriomes that consist of giant cells termed bacteriocytes. The bacteriocyte cytoplasm is tightly packed with endosymbiotic bacteria. Ultrastructural observations have shown that the bacteria Buchnera aphidicola (primary symbiont of aphids) present in various species are characterized by significant differences in both size and organization of their cytoplasm. In the aphids, Prociphilus fraxini, Sipha (Rungsia) maydis, Thelaxes dryophila, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria, Eulachnus rileyi and Schizolachnus pineti, in addition to Buchnera aphidicola, secondary endosymbionts are also present. The bacteriocytes containing secondary endosymbionts are less numerous than those with Buchnera. In Eulachnus rileyi (Lachnidae), in addition to primary and secondary endosymbionts, there is a third type of microorganism. In all species examined both the primary and secondary endosymbionts are transovarially transmitted from mother to offspring.

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“…For example, the aphid Cinara cedri contains Buchnera along with a second obligate symbiont, Serratia symbiotica, which lives in a distinct type of bacteriocyte (87)(88)(89). The acquisition of S. symbiotica coincides with further gene loss in Buchnera: The C. cedri Buchnera genome is substantially smaller and lacks several amino acid biosynthetic genes present in other Buchnera (55).…”

Section: Escaping the Hazards Of Symbiosis: Acquiring Novel Symbiosesmentioning

confidence: 99%

“…For color-coded lines, see Inset legend. Host phylogeny represents the most recent understanding, but placement of certain lineages (e.g., the Coleorrhyncha and Heteroptera) is uncertain (12,89). Ancestral symbiont names are in boxes along their lineage; in some cases, the same symbiont lineage has different names in different insect clades.…”

Section: Escaping the Hazards Of Symbiosis: Acquiring Novel Symbiosesmentioning

confidence: 99%

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

Bennett

Moran

2015

Proc. Natl. Acad. Sci. U.S.A.

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436

515

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Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sapfeeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphidBuchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.Buchnera | aphid | Muller's ratchet | selection levels | coevolution

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Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae

Cited by 81 publications

References 39 publications

Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium

Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

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