The impact of clonal mixing on the evolution of social behaviour in aphids

Abstract

Reports of substantial clonal mixing measured in social aphid colonies seem, on the face of it, to rule out population structure as an explanation of this enigmatic insect's social behaviour. To clarify how selection operates in aphids, and to disentangle direct and indirect fitness components, we present a model of the life cycle of a typical colony-dwelling aphid. The model incorporates ecological factors and includes a trade-off between investing in social behaviour and investing in reproduction. Our focus on inclusive fitness contrasts with previous approaches that optimize colony output. Through deriving a variant of Hamilton's rule, we show that a simple relationship can be established between the patch-carrying capacity and immigration rates into patches. Our results indicate that the levels of clonal mixing reported are not inconsistent with social behaviour. We discuss our model in terms of the evolutionary origins of social behaviour in aphids.

Figure 1.

The typical aphid life cycle showing the movement of aphids between different habitats. Fundatrices hatch and find patches to start colonies where they reproduce parthenogenetically for several generations. After a period of several weeks, the colonies open and alatae are released. In most species, these move to a second host where they grow for further generations. Eventually aphids return to the overwintering site where eggs are laid, which hatch at the beginning of the next cycle.

Figure 2.

The ESS carrying capacity , for the single-fundatrix case, as a function of the proportion of immigrants per patch. We plot , m, where . Here we have plotted as a percentage of the value when patches are at optimum carrying capacity K₀.

Figure 3.

The relatedness for different levels of fundatrices and immigrants shows how immigration decreases the relatedness in both cases. (a) When there is a single fundatrix, the proportion of patches with fundatrices has no impact. (b) The impact of low- to mid-levels of immigration is not that significant compared with the level of patch colonization.

Figure 4.

The mathematical treatment is largely similar to the simulation results. Comparing data points that have the same intrinsic migration level γ (linked with arrows), we see there is negligible impact to the ESS growth rate () from spending extra time on the patches. The error bar is shown for standard error greater than 0.005. The dotted line shows the value of r_max for this parameter set: K₀ = 1000, K_r = 5000 and η = 0.003. Open circles, mathematical prediction; crosses, immigrants placed at start; open squares, growth stops at carrying capacity; triangles, growth over fixed period.