Social immunity as a driver of life-history evolution in eusocial species

Eusociality is accompanied by puzzling lifespan phenotypes that challenge classic theories of aging. In eusocial species, breeders age more slowly than non-breeders while sharing the same genomes. A notable exception is the naked mole-rat, in which all castes show negligible actuarial senescence. We show that both patterns can be explained with a single epidemiological model. Chronic parasites that reduce worker productivity can drive the evolution of shorter lifespan in workers, but not in queens. A genetic program that triggers the death of infected workers can evolve as an efficient alternative strategy for controlling pathogens, thereby reducing selection for shorter lifespan. However, in the presence of benign pathogens, this program results in excessive deaths and becomes too costly. Therefore, the composition of the pathogen mixture defines optimal life histories in eusocial communities: species exposed to a broad pathogen repertoire evolve caste differences in lifespan, whereas species occupying pathogen-poor environments are predicted to die rapidly upon infection and experience negligible aging. This framework links social immunity to life-history evolution and yields testable predictions for the pathogen control hypothesis of aging.