Ecological and evolutionary processes may become intertwined when they operate on similar time scales. Here we show ecological–evolutionary dynamics between parasitoids and aphids containing heritable symbionts that confer resistance against parasitism. In a large-scale field experiment, we manipulated the aphid’s host plant to create ecological conditions that either favoured or disfavoured the parasitoid. The result was rapid evolutionary divergence of aphid resistance between treatment populations. Consistent with ecological–evolutionary dynamics, the resistant aphid populations then had reduced parasitism and increased population growth rates. We fit a model to quantify costs (reduced intrinsic rates of increase) and benefits of resistance. We also performed genetic assays on 5 years of field samples that showed persistent but highly variable frequencies of aphid clones containing protective symbionts; these patterns were consistent with simulations from the model. Our results show (1) rapid evolution that is intertwined with ecological dynamics and (2) variation in selection that prevents traits from becoming fixed, which together generate self-perpetuating ecological–evolutionary dynamics.
This is a preview of subscription content, access via your institution
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Experimental and observational data that support the findings of this study have been deposited in figshare.com at https://doi.org/10.6084/m9.figshare.11828865.v1.
Codes used for analyses in this study have been deposited in figshare.com at https://doi.org/10.6084/m9.figshare.11828865.v1
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).
Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, 1986).
Thompson, J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).
Schoener, T. W. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331, 426–429 (2011).
Pelletier, F., Garant, D. & Hendry, A. P. Eco-evolutionary dynamics. Phil. Trans. R. Soc. Lond. B 364, 1483–1489 (2009).
Hairston, N. G., Ellner, S. P., Geber, M. A., Yoshida, T. & Fox, J. A. Rapid evolution and the convergence of ecological and evolutionary time. Ecol. Lett. 8, 1114–1127 (2005).
Nosil, P. et al. Natural selection and the predictability of evolution in Timema stick insects. Science 359, 765–770 (2018).
Auld, S. K. J. R. et al. Variation in costs of parasite resistance among natural host populations. J. Evol. Biol. 26, 2479–2486 (2013).
Duffy, M. A. et al. Ecological context influences epidemic size and parasite-driven evolution. Science 335, 1636–1638 (2012).
Travis, J. et al. in Eco-Evolutionary Dynamics Vol. 50 (eds Moya-Laraño, J. et al.) 1–40 (Academic Press, 2014).
Schaffner, L. R. et al. Consumer-resource dynamics is an eco-evolutionary process in a natural plankton community. Nat. Ecol. Evol. 3, 1351–1358 (2019).
De Meester, L. et al. Analysing eco-evolutionary dynamics: the challenging complexity of the real world. Funct. Ecol. 33, 43–59 (2019).
Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003).
Papkou, A. et al. The genomic basis of Red Queen dynamics during rapid reciprocal host–pathogen coevolution. Proc. Natl Acad. Sci. USA 116, 923–928 (2019).
Saccheri, I. & Hanski, I. Natural selection and population dynamics. Trends Ecol. Evol. 21, 341–347 (2006).
Govaert, L. et al. Eco-evolutionary feedbacks—theoretical models and perspectives. Funct. Ecol. 33, 13–30 (2019).
Siepielski, A. M., DiBattista, J. D. & Carlson, S. M. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12, 1261–1276 (2009).
Carroll, S. P., Hendry, A. P., Reznick, D. N. & Fox, C. W. Evolution on ecological time-scales. Funct. Ecol. 21, 387–393 (2007).
Lankau, R. A., Nuzzo, V., Spyreas, G. & Davis, A. S. Evolutionary limits ameliorate the negative impact of an invasive plant. Proc. Natl Acad. Sci. USA 106, 15362–15367 (2009).
van den Bosch, R., Schlinger, E. I., Hall, J. C. & Puttler, B. Studies on succession, distribution and phenology of imported parasites of Therioaphis trifolii (Monell) in southern California. Ecology 45, 602–621 (1964).
Mackauer, M. Growth and developmental interactions in some aphids and their hymenopterous parasites. J. Insect Physiol. 32, 275–280 (1986).
Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247–266 (2010).
Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803–1807 (2003).
Meisner, M. H., Harmon, J. P. & Ives, A. R. Temperature effects on long-term population dynamics in a parasitoid-host system. Ecol. Monogr. 84, 457–476 (2014).
Snyder, W. E. & Ives, A. R. Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84, 91–107 (2003).
Ives, A. R. & Settle, W. H. Metapopulation dynamics and pest control in agricultural systems. Am. Nat. 149, 220–246 (1997).
Bender, E. A., Case, T. J. & Gilpin, M. E. Perturbation experiments in community ecology: theory and practice. Ecology 65, 1–13 (1984).
Oliver, K. M. & Higashi, C. H. V. Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Curr. Opin. Insect Sci. 32, 1–7 (2019).
Martinez, A. J., Doremus, M. R., Kraft, L. J., Kim, K. L. & Oliver, K. M. Multi-modal defences in aphids offer redundant protection and increased costs likely impeding a protective mutualism. J. Anim. Ecol. 87, 464–477 (2018).
Oliver, K. M., Degnan, P. H., Hunter, M. S. & Moran, N. A. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992–994 (2009).
Martinez, A. J., Kim, K. L., Harmon, J. P. & Oliver, K. M. Specificity of multi-modal aphid defenses against two rival parasitoids. PLoS ONE 11, e0154670 (2016).
Rock, D. I. et al. Context-dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 27, 2039–2056 (2018).
Doremus, M. R. & Oliver, K. M. Aphid heritable symbiont exploits defensive mutualism. Appl. Environ. Microbiol. 83, AEM.03276-16 (2017).
Oliver, K. M., Smith, A. H. & Russell, J. A. Defensive symbiosis in the real world—advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28, 341–355 (2014).
Losey, J. E., Ives, A. R., Harmon, J., Brown, C. & Ballantyne, F. A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388, 269–272 (1997).
Harmon, J., Losey, J. & Ives, A. R. The use of color vision in Coccinellidae. Oecologia 115, 287–292 (1998).
Langley, S. A., Tilmon, K. J., Cardinale, B. J. & Ives, A. R. Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae) alters individual fixed preferences for pea aphid color morphs. Oecologia 150, 172–179 (2006).
Tomasetto, F., Tylianakis, J. M., Reale, M., Wratten, S. & Goldson, S. L. Intensified agriculture favors evolved resistance to biological control. Proc. Natl Acad. Sci. USA 114, 3885–3890 (2017).
Hufbauer, R. A. & Roderick, G. K. Microevolution in biological control: mechanisms, patterns, and processes. Biol. Control 35, 227–239 (2005).
Mills, N. J. Rapid evolution of resistance to parasitism in biological control. Proc. Natl Acad. Sci. USA 114, 3792–3794 (2017).
Vorburger, C. & Perlman, S. J. The role of defensive symbionts in host–parasite coevolution. Biol. Rev. Camb. Philos. Soc. 93, 1747–1764 (2018).
Caltagirone, L. E. Landmark examples in classical biological control. Annu. Rev. Entomol. 26, 213–232 (1981).
Desneux, N. et al. Intraspecific variation in facultative symbiont infection among native and exotic pest populations: potential implications for biological control. Biol. Control 116, 27–35 (2018).
Kach, H., Mathe-Hubert, H., Dennis, A. B. & Vorburger, C. Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids. Evol. Appl. 11, 220–230 (2018).
Dennis, A. B., Patel, V., Oliver, K. M. & Vorburger, C. Parasitoid gene expression changes after adaptation to symbiont-protected hosts. Evolution 71, 2599–2617 (2017).
Barbosa, P. in Conservation Biological Control (ed. Barbosa, P.) 39–54 (Academic Press, 1998).
Snyder, W. E., Chang, G. C. & Prasad, R. P. in Ecology of Predator–Prey Interactions (eds Barbosa, P. & Castellanos, I.) 324–343 (Oxford Univ. Press, 2004).
Tscharntke, T. et al. When natural habitat fails to enhance biological pest control—five hypotheses. Biol. Conserv. 204, 449–458 (2016).
Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B 275, 293–299 (2008).
Lynn-Bell, N. L., Strand, M. R. & Oliver, K. M. Bacteriophage acquisition restores protective mutualism. Microbiology 165, 985–989 (2019).
Henry, L. M. et al. Horizontally transmitted symbionts and host colonization of ecological niches. Curr. Biol. 23, 1713–1717 (2013).
Gehrer, L. & Vorburger, C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol. Lett. 8, 613–615 (2012).
Li, Q., Fan, J., Sun, J., Wang, M.-Q. & Chen, J. Plant-mediated horizontal transmission of Hamiltonella defensa in the wheat aphid Sitobion miscanthi. J. Agric. Food Chem. 66, 13367–13377 (2018).
Moran, N. A. & Dunbar, H. E. Sexual acquisition of beneficial symbionts in aphids. Proc. Natl Acad. Sci. USA 103, 12803–12806 (2006).
Brandt, J. W., Chevignon, G., Oliver, K. M. & Strand, M. R. Culture of an aphid heritable symbiont demonstrates its direct role in defence against parasitoids. Proc. R. Soc. B. 284, 20171925 (2017).
Martinez, A. J., Weldon, S. R. & Oliver, K. M. Effects of parasitism on aphid nutritional and protective symbioses. Mol. Ecol. 23, 1594–1607 (2014).
Russell, J. A. et al. Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol. Ecol. 22, 2045–2059 (2013).
Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E. & Ochman, H. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc. Natl Acad. Sci. USA 102, 16919–16926 (2005).
Ives, A. R. et al. Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. Am. Nat. 154, 652–673 (1999).
Ives, A. R. & Dakos, V. Detecting dynamical changes in nonlinear time series using locally linear state-space models. Ecosphere 3, art58 (2012).
Harvey, A. C. Forecasting, Structural Time Series Models and the Kalman Filter (Cambridge Univ. Press, 1989).
Rauwald, K. S. & Ives, A. R. Biological control in disturbed agricultural systems and the rapid re-establishment of parasitoids. Ecol. Appl. 11, 1224–1234 (2001).
Olson, A. C., Ives, A. R. & Gross, K. Spatially aggregated parasitism on pea aphids, Acyrthosiphon pisum, caused by random foraging behavior of the parasitoid Aphidius ervi. Oikos 91, 66–76 (2000).
Caswell, H. Matrix Population Models (Sinauer Associates, 1989).
Caillaud, M. C. & Losey, J. E. Genetics of color polymorphism in the pea aphid, Acyrthosiphon pisum. J. Insect Sci. 10, 95 (2010).
This work could not have been done without help from the UW Arlington Agricultural Research Station staff, in particular J. Breuer and M. Bertram. Many undergraduate, graduate and postdoctoral students helped to collect and administer our long-term data. Funding was provided by NASA/NSF-DEB Dimensions of Biodiversity grant nos. 1240804 and 1240892.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
a, Photograph of a hoop house experimental screen cage with lucerne harvested asynchronously in four strips (photo credit A. R. Ives). b, Google Earth satellite image of the four hoop houses in September, 2010. (A different experiment was being performed that compared treatments within and outside the hoop houses).
Normal-Poisson GLMM for the number of aphids recovered in the assays for resistance depending on whether the line contains or does not contain Hamiltonella-APSE3 (Ham+ or Ham-) and whether parasitoids were added (parasitoid+) or not (parasitoid-), with random effects for the focal line, the competing line and the observation. See Supplementary Information: ‘Assays for resistance in experimental aphid clones’.
Extended Data Fig. 3 Experiment to measure phenotypic resistance among Hamiltonella-containing aphid clones.
In a field experiment investigating resistance to parasitism, final aphid abundances for clones with and without Hamiltonella-APSE3 (Ham+ and Ham-) when parasitic wasps were not supplemented (F) or were supplemented (T). In the top panel all trials are included, whereas in the bottom panel only trials containing the clones used to inoculate the hoop houses are included. See Supplementary Information: ‘Assays for resistance in experimental aphid clones’.
Numbers of assayed pea aphids containing Hamiltonella and the numbers containing no symbionts in hoop houses and cages within hoop houses at three sampling dates. See ‘Hoop house experiment’.
Extended Data Fig. 5 Likelihood function for the model fit to hoop house data from summer-autumn 2015 graphed for the benefits and costs of resistance.
The benefit of resistance is the probability that an aphid attacked by a parasitoid kills the parasitoid egg, given by (1—b) in the fitted model. The cost of resistance is the proportional reduction in fecundity, given by (1—c). The maximum likelihood estimates of both parameters are marked by the red cross and the contour lines are at intervals of ΔlogLik = 5.99/2; 5.99 is the value of a chi-square distribution with df = 2, so the first contour corresponds to the joint approximate 95% confidence interval given by a Likelihood Ratio Test.
Extended Data Fig. 6 Analyses of changes in the proportion of pea aphid clones containing Hamiltonella-APSE3 relative to uninfected clones between 23 September, 2015, and 22 April, 2016.
a, Binomial ANOVA analysis of the proportion of aphid clones with Hamiltonella-APSE3, showing a decrease in infections over winter. b, Binomial ANOVA analysis of the proportion of aphid clones with Hamiltonella-APSE3 in spring including the proportion infected in autumn as a predictor, showing that harvesting treatment (synchronous versus asynchronous) does not affect this change. See Supplementary Information: ‘Hoop house experiment—Additional statistical analyses (ii) Levels of resistance’.
Extended Data Fig. 7 Regional stability of the simulation model showing the frequency of resistant aphid clones (black line) and the proportion parasitism (red line) calculated from all 40 simulated fields.
To illustrate regional dynamics of the simulation model (Fig. 3), we removed the log-normal variation in aphid survival within fields and iterated the model for 4000 days. On days 667 and 2667, a perturbation was applied in which the proportion of the resistant clone was sharply increased. This caused parasitism to decrease, and with decreased parasitism selection favoured the non-resistant clone. After roughly 1000 days the proportion of resistant clones and proportion parasitism returned to their regional equilibrium values.
Model parameter estimates. Parameter estimates from the state-space model fit to the hoop house experiment for summer-autumn 2015 and spring 2016. See ‘Model of resistance fitted to hoop house experiment data’ and Supplementary Information: ‘Model of resistance fitted to hoop house experiment data—Model fitting’.
About this article
Cite this article
Ives, A.R., Barton, B.T., Penczykowski, R.M. et al. Self-perpetuating ecological–evolutionary dynamics in an agricultural host–parasite system. Nat Ecol Evol 4, 702–711 (2020). https://doi.org/10.1038/s41559-020-1155-0
Nature Ecology & Evolution (2022)
Nature Ecology & Evolution (2020)