Oh sister, where art thou? Spatial population structure and the evolution of an altruistic defence trait

TL;DR

This study investigates how small-scale population structure influences the evolution of altruistic defense behaviors in enslaved ant workers, combining mathematical modeling and genetic analysis to reveal kin selection effects.

Contribution

It demonstrates that local relatedness within host populations can promote altruistic rebellion behaviors through kin selection, supported by a mathematical model and genetic data.

Findings

Enslaved workers are more related to nearby host nests within raiding range.

Small-scale population structure facilitates evolution of altruistic defense traits.

Kin selection likely drives rebellion behavior in enslaved ant workers.

Abstract

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post-enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites' offspring. Since enslaved workers do not reproduce, they gain no direct fitness benefit from this 'rebellion' behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to 'rebel' nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers' killing behaviour. We use a simple mathematical model to examine whether the small-scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small-scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of 'rebellion' by kin selection.