Colonies of social insects contain large amounts of resources often exploited by specialized social parasites. While some termite species host numerous parasitic arthropod species, called termitophiles, others host none. The reason for this large variability remains unknown. Here we report that the evolution of termitophily in rove beetles is linked to termite nesting strategies. We compared one-piece nesters, whose entire colony life is completed within a single wood piece, to foraging species, which exploit multiple physically separated food sources. Our epidemiological model predicts that characteristics related to foraging (e.g., extended colony longevity and frequent interactions with other colonies) increase the probability of parasitism by termitophiles. We tested our prediction using literature data. We found that foraging species are more likely to host termitophilous rove beetles than one-piece nesters: 99.6% of known termitophilous species were associated with foraging termites, while 0.4% were associated with one-piece nesters. Notably, the few one-piece nesting species hosting termitophiles were those having foraging potential and access to soil. Our phylogenetic analyses confirmed that termitophily primarily evolved with foraging termites. These results highlight that the evolution of complex termite societies fostered social parasitism, explaining why some species have more social parasites than others.

Funding provided by: Japan Society for the Promotion of ScienceCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001691Award Number: 20J00660Funding provided by: Japan Society for the Promotion of ScienceCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001691Award Number: 19K16220

All data were collected through a literature survey. Please see the method section of the paper in detail.