Costs and benefits of a superinfection of facultative symbionts in aphids
Open accessAbstract
Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola . Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi . Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host–symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Insects can also carry facultative (secondary) endosymbionts whose fitness effects on their hosts can be variable and complex.
“Insects can also carry facultative (secondary) endosymbionts whose fitness effects on their hosts can be variable and complex (Oliver et al. 2006(Oliver et al. , 2009;;Degnan et al. 2009;Burke et al. 2010).”
From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Oliver et al. 2006
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
No references could be resolved yet.
Research works printed but not linked: 36
- Chen, D. Q. & Purcell, A. H. 1997 Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol. 34 , 220-225. (doi:10.1007/s002849900172) · DOI
- Chen, D. Q., Campbell, B. C. & Purcell, A. H. 1996 A new Rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr. Microbiol. 33 , 123-128. (doi:10.1007/s002849900086) · DOI
- Digilio, M. C., Isidoro, N., Tremblay, E. & Pennacchio, F. 2000 Host castration by Aphidius ervi venom proteins. J. Insect Physiol. 46 , 1041-1050. (doi:10.1016/S00221910(99)00216-4) · DOI
- Distel, D. L., Beaudoin, D. J. & Morrill, W . 2002 Coexistence of multiple proteobacterial endosymbionts in the gills of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl. Environ. Microbiol. 68 , 6292-6299. (doi:10.1128/AEM.68.12.6292-6299.2002) · DOI
- Dubilier, N. et al . 2001 Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411 , 298-302. (doi:10.1038/35077067) · DOI
- Eastop, V. F. 1966 A taxonomic study of Australian Aphidoidea (Homoptera). Aust. J. Zool. 14 , 399-592. (doi:10.1071/ZO9660399) · DOI
- Frank, S. A. 1998 Dynamics of cytoplasmic incompatibility with multiple Wolbachia infections. J. Theor. Biol. 192 , 213-218. (doi:10.1006/jtbi.1998.0652) · DOI
- Fukatsu, T. & Nikoh, N. 2000 Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl. Environ. Microbiol. 66 , 643-650. (doi:10.1128/AEM.66.2.643-650.2000) · DOI
- Fukatsu, T., Nikoh, N., Kawai, R. & Koga, R. 2000 The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 66 , 2748-2758. (doi:10.1128/AEM.66.7.27482758.2000) · DOI
- Fukatsu, T., Tsuchida, T., Nikoh, N. & Koga, R. 2001 Spiroplasma symbiont of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67 , 1284-1291. (doi:10.1128/AEM.67.3.1284-1291.2001) · DOI
- Ijichi, N., Kondo, N., Matsumoto, R., Shimada, M., Ishikawa, H. & Fukatsu, T. 2002 Internal spatiotemporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle Callosobruchus chinensis (Coleoptera: Bruchidae). Appl. Environ. Microbiol. 68 , 4074-4080. (doi:10.1128/AEM.68.8.4074-4080.2002) · DOI
- Ikeda, T., Ishikawa, H. & Sasaki, T. 2003 Regulation of Wolbachia density in the Mediterranean flour moth Ephestia kuehniella , and the almond moth, Cadra cautella . Zool. Sci. 20 , 153-157. (doi:10.2108/zsj.20.153) · DOI
- Koga, R., Tsuchida, T. & Fukatsu, T. 2003 Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. B 270 , 2543-2550. (doi:10.1098/rspb.2003.2537) · DOI
- Lerat, E. & Moran, N. A. 2004 Evolutionary history of quorum-sensing systems in bacteria. Mol. Biol. Evol. 21 , 903-913. (doi:10.1093/molbev/msh097) · DOI
- Mackauer M. 1968 ' Acyrthosiphon pisum (Harris) pea aphid (Homoptera: Aphididae)'. Biological Control programmes against insects and weeds in Canada 1959-1968 . Technical communication, no. 4, pp. 3-11. Trinidad: Commonwealth Institute of Biological Control.
- McGraw, E. A., Merritt, D. J., Droller, J. N. & O'Neill, S. L. 2002 Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl Acad. Sci. USA 99 , 2918-2923. (doi:10.1073/pnas.052466499) · DOI
- Mira, A. & Moran, N. A. 2002 Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44 , 137-143. (doi:10.1007/s00248-002-0012-9) · DOI
- Montllor, C. B., Maxmen, A. & Purcell, A. H. 2002 Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27 , 189-195. (doi:10.1046/j.1365-2311.2002.00393.x) · DOI
- Moran, N. A., Kaplan, M. E., Gelsey, M. J., Murphy, T. G. & Scholes, E. A. 1999 Phylogenetics and evolution of the aphid genus Uroleucon based on mitochondrial and nuclear DNAsequences. Syst. Entomol. 24 , 85-93. (doi:10.1046/j. 1365-3113.1999.00076.x) · DOI
- Moran, N. A., Degnan, P. A., Santos, S. R., Dunbar, H. E. & Ochman, H. 2005 a The players in a mutualistic symbiosis: insects, bacteria, viruses and virulence genes. Proc. Natl Acad. Sci. USA 102 , 16919-16926.
- Mouton, L., Henri, H., Bouletreau, M. & Vavre, F. 2003 Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 12 , 3459-3465. (doi:10.1046/j.1365-294X.2003.02015.x) · DOI
- Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. 2003 Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100 , 1803-1807. (doi:10.1073/pnas.0335320100) · DOI
- Oliver, K. M., Moran, N. A. & Hunter, M. S. 2005 Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl Acad. Sci. USA 102 , 12795-12800.
- O'Neill, S. L., Giordano, R., Colbert, A. M. E., Karr, T. L. & Robertson, H. M. 1992 16S rRNA Phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl Acad. Sci. USA 89 , 2699-2702.
- Prosser, W. A. & Douglas, A. E. 1991 The aposymbiotic aphid-an analysis of chlortetracycline-treated pea aphid Acyrthosiphon pisum . J. Insect Physiol. 37 , 713-719. (doi:10.1016/0022-1910(91)90104-8) · DOI
- Russell, J. A., Latorre, A., Sabater-Munoz, B., Moya, A. & Moran, N. A. 2003 Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12 , 1061-1075. (doi:10.1046/j. 1365-294X.2003.01780.x) · DOI
- Russell, J. A. & Moran, N. A. 2006 Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. B 273 , 603-610. (doi:10.1098/rspb.2005.3348) · DOI
- Sandstro ¨m, J. P., Russell, J. A., White, J. P. & Moran, N. A. 2001 Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10 , 217-228. (doi:10.1046/j.1365-294X.2001.01189.x) · DOI
- Subandiyah, S., Nikoh, N., Tsuyumu, S., Somowiyarjo, S. & Fukatsu, T. 2000 Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera: Psylloidea). Zool. Sci. 17 , 983-989. (doi:10.2108/zsj.17.983) · DOI
- Terry, R. S. et al . 2004 Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc. R. Soc. B 271 , 1783-1789. (doi:10.1098/rspb.2004.2793) · DOI
- Tsuchida, T., Koga, R. & Fukatsu, T. 2004 Host plant specialization governed by facultative symbiont. Science 303 , 1989-1989. (doi:10.1126/science.1094611) · DOI
- von Dohlen, C. D., Kohler, S., Alsop, S. T. & McManus, W. R. 2001 Mealybug b -proteobacterial endosymbionts contain g -proteobacterial symbionts. Nature 412 , 433-436. (doi:10.1038/35086563) · DOI · Paper page
- Weeks, A. R., Velten, R. & Stouthamer, R. 2003 Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc. R. Soc. B 270 , 1857-1865. (doi:10.1098/rspb.2003.2425) · DOI
- Werren, J. H. & O'Neil, S. L. 1997 The evolution of heritable symbionts. In Influential passengers: inherited micro-organisms and arthropod reproduction (ed. S. L. O'Neill, A. A. Hoffman & J. H. Werren), pp. 2-10. Oxford, UK: Oxford University Press.
- Werren, J. H. & Windsor, D. M. 2000 Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. B 267 , 1277-1285. (doi:10.1098/rspb.2000. 1139) · DOI
- Zchori-Fein, E. & Perlman, S. J. 2004 Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13 , 2009-2016. (doi:10.1111/j.1365-294X.2004.02203.x) · DOI
Cited by
Sorted by citations
RELAX: Detecting Relaxed Selection in a Phylogenetic Framework
Wertheim, J. O., Murrell, B., Smith, M. D., Kosakovsky Pond, S. L., & Scheffler, K. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msu400 · Cited by 778 · see citing works
- Authors
- Oliver, K. M., Moran, N. A., & Hunter, M. S.
- Affiliations
- University of Arizona (US)
- Corresponding author
- Oliver, Kerry M
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2006-02-15
- Volume
- 273
- Issue
- 1591
- Pages
- 1273-1280
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC1560284
- OpenAlex
- W2148958822
- Cited by
- 267
- References
- 0
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 10 · 2023: 6 · 2022: 11 · 2021: 11 · 2020: 13 · 2019: 17 · 2018: 16 · 2017: 19 · 2016: 24 · 2015: 8 · 2014: 19 · 2013: 18 · 2012: 16
- FWCI
- 14.32
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Agriculture
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Keywords
- superinfection, facultative symbionts, secondary symbionts, Acyrthosiphon pisum, Serratia symbiotica, Hamiltonella defensa, Buchnera aphidicola, parasitoid resistance, Aphidius ervi, symbiont interactions, fecundity cost, symbiont density, host-symbiont interactions, symbiont distribution
- MeSH terms
- Animals, Aphids, Enterobacteriaceae, Fertility, Immunity, Innate, Phenotype, Serratia, Symbiosis, Utah
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review