Self-perpetuating ecological–evolutionary dynamics in an agricultural host–parasite system 

Ives et al. 2020

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.

Field experiment showing eco–evo dynamics. Between mid-summer and autumn 2015 (panels on the left), the asynchronous harvesting treatment was applied in two hoop houses to maintain aphid habitat and increased parasitoid populations (top two panels) or synchronously to decrease parasitism pressure on aphids (bottom two panels). We counted aphids (solid and dashed black lines for the two hoop houses in each treatment) by visual inspection of 500 stems per cage; s.e.m. bars are given but in some cases are covered by the dots. Our index of parasitism (red lines) is the number of mummies as a proportion of the number of mummies and aphids. Peak parasitism rates (on 20 and 26 August and 2 September 2015) were higher in the asynchronous hoop houses (P = 0.007, Supplementary Information). The narrow panels give the estimated demographic rates (for the hoop houses in the panels above them) from the fitted model (Extended Data Fig. 8). The estimated daily parasitoid attack rates (a(t) in equation (2)) is given in red and the densityindependent relative aphid survival (z(t) in equation (2)) is given in blue, with solid and dashed lines corresponding to the two replicates. Note that the relative aphid survival is scaled to the maximum estimated survival in 2015, so values greater than 1 in 2016 imply higher survival than the 2015 maximum. The estimated proportion of resistant clones is given by black lines and the black points with s.e.m. give the proportion of Hamiltonella–APSE3 clones from the genetic symbiont surveys.

https://www.nature.com/articles/s41559-020-1155-0

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