Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups

Contrary to the expectations of kin selection theory, intracolony relatedness in eusocial insects is often low. We examined the idea that associations of low relatedness (high genetic variability) may be advantageous because of negative frequency-dependent selection on common host phenotypes by rapidly evolving parasites and pathogens. Using the natural host-parasite system of the bumble bee Bombus terrestris and its intestinal trypanosome Crithidia bombi, we investigated the transmission properties of parasites in host groups. Within naturally infested nests and in artificially constructed groups of workers, prevalence of infestation increased with time of exposure (Table 1). The susceptibility of isolated groups of workers to the parasites to which they were exposed differed with identity and natural infestation of their nest of origin (Table 2). In addition, those workers that were related to the individual introducing an infection to their group were more likely to become infested than were unrelated workers (Table 3). Although the bumble bee workers in experimental boxes appeared to differ in behavior toward kin and non-kin, making more physical contacts with kin, we found no discernible relationship between number of physical contacts and prevalence of infestation in a group. Therefore, we conclude that differences in parasite transmission reflected interactions among different host and parasite phenotypes. This system thus demonstrates the factors necessary for negative frequency-dependent selection by parasites on common host phenotypes - variability for susceptibility and infectiousness in host and parasite populations and similarity for these traits among related individuals. If, as we show here, high genetic relatedness within groups enhances parasite transmission, kin directed altruism may increase the risk of contracting parasites and infectious diseases. Therefore, parasites and pathogens may be an important force moderating the genetic structure of social groups.