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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.

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