Animal-associated microbial communities have important effects on host phenotypes. Individuals within and among species differ in the strains and species of microbes that they harbour, but how natural selection shapes the distribution and abundance of symbionts in natural populations is not well understood. Symbionts can be beneficial in certain environments but also impose costs on their hosts. Consequently, individuals that can or cannot associate with symbionts will be favoured under different ecological circumstances. As a result, we predict that individuals within a species vary in terms of how well they accept and maintain symbionts. In pea aphids, the frequency of endosymbionts varies among host-plant-associated populations ('biotypes'). We show that aphid genotypes from different biotypes vary in how well they accept and maintain symbionts after horizontal transfer. We find that aphids from biotypes that frequently harbour symbionts are better able to associate with novel symbionts than those from biotypes that less frequently harbour symbionts. Intraspecific variation in the ability of hosts to interact with symbionts is an understudied factor explaining patterns of host-symbiont association.

Biology Centre CAS Ceske Budejovice Czech Republic

Department of Biology Emory University Atlanta GA USA

Department of Zoology University of Oxford Oxford UK

See more in PubMed

Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34. ( 10.1146/annurev-ento-010814-020822) PubMed DOI PMC

Ferrari J, Vavre F. 2011. Bacterial symbionts in insects or the story of communities affecting communities. Phil. Trans. R. Soc. B 366, 1389–1400. ( 10.1098/rstb.2010.0226) PubMed DOI PMC

Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. 2010. Adaptation via symbiosis: recent spread of a PubMed DOI

Himler AG, et al. 2011. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332, 254–256. ( 10.1126/science.1199410) PubMed DOI

Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L. 2013. PubMed DOI PMC

Jaenike J. 2012. Population genetics of beneficial heritable symbionts. Trends Ecol. Evol. 27, 227–233. ( 10.1016/j.tree.2011.10.005) PubMed DOI

Login FH, Balmand S, Vallier A, Vincent-Monegat C, Vigneron A, Weiss-Gayet M, Rochat D, Heddi A. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334, 362–365. ( 10.1126/science.1209728) PubMed DOI

Haselkorn TS, Cockburn SN, Hamilton PT, Perlman SJ, Jaenike J. 2013. Infectious adaptation: potential host range of a defensive endosymbiont in PubMed DOI

Łukasik P, Guo H, van Asch M, Henry LM, Godfray HCJ, Ferrari J. 2015. Horizontal transfer of facultative endosymbionts is limited by host relatedness. Evolution 69, 2757–2766. ( 10.1111/evo.12767) PubMed DOI

Haselkorn TS, Markow TA, Moran NA. 2009. Multiple introductions of the PubMed DOI

Duron O, Wilkes TE, Hurst GDD. 2010. Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol. Lett. 13, 1139–1148. ( 10.1111/j.1461-0248.2010.01502.x) PubMed DOI

Henry LM, Peccoud J, Simon J-C, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ. 2013. Horizontally transmitted symbionts and host colonization of ecological niches. Curr. Biol. 23, 1713–1717. ( 10.1016/j.cub.2013.07.029) PubMed DOI PMC

McLean AHC, Parker BJ, Hrček J, Henry LM, Godfray HCJ. 2016. Insect symbionts in food webs. Phil. Trans. R. Soc. B 371, 20150325 ( 10.1098/rstb.2015.0325) PubMed DOI PMC

Hrček J, McLean AHC, Godfray HCJ. 2016. Symbionts modify interactions between insects and natural enemies in the field. J. Anim. Ecol. 85, 1423–1646. ( 10.1111/1365-2656.12586) PubMed DOI PMC

Peccoud J, Ollivier A, Plantegenest M, Simon J-C. 2009. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc. Natl Acad. Sci. USA 106, 7495–7500. ( 10.1073/pnas.0811117106) PubMed DOI PMC

Ferrari J, West JA, Via S, Godfray HCJ. 2012. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66, 375–390. ( 10.1111/j.1558-5646.2011.01436.x) PubMed DOI

McLean AHC, van Asch M, Ferrari J, Godfray HCJ. 2011. Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc. R. Soc. B 278, 760–766. ( 10.1098/rspb.2010.1654) PubMed DOI PMC

Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. ( 10.18637/jss.v067.i01) DOI

R Core Development Team. 2015.

Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biom. J. 50, 346–363. ( 10.1002/bimj.200810425) PubMed DOI

Peccoud J, Simon J-C, McLaughlin HJ, Moran NA. 2009. Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proc. Natl Acad. Sci. USA 106, 16 315–16 320. ( 10.1073/pnas.0905129106) PubMed DOI PMC

Parker BJ, McLean A, Hrcek J, Gerardo N, Godfray HCJ. 2017. Data from: Establishment and maintenance of aphid endosymbionts after horizontal transfer is dependent on host biotype. PubMed DOI PMC

Establishment and maintenance of aphid endosymbionts after horizontal transfer is dependent on host genotype

See more in PubMed

Dryad
10.5061/dryad.k50h1