Reproduction by worker-derived kings under natural conditions in the termite Reticulitermes speratus.

A defining feature of eusociality is the presence of a lifelong sterile caste, such as workers and soldiers, that forgo reproduction entirely. In many species, however, workers are not absolutely sterile but are instead functionally sterile—they retain reproductive potential that can be expressed under certain conditions. Why this potential persists despite the evolutionary expectation of trait loss remains an open question. In this study, we present the first field-based evidence that worker-derived male reproductives, previously known only from laboratory observations, can successfully reproduce under natural conditions in the subterranean termite Reticulitermes speratus. A survey of 702 field colonies identified one colony containing only worker-derived kings. Microsatellite genotyping confirmed that these individuals reproduced via mother–son mating (i.e., within-colony inbreeding), and the caste fate of their offspring matched the expected pattern for matings between worker-derived kings and nymph-derived queens. Importantly, no male nymphs—the usual precursors of male reproductives—were present in the colony. Further investigation revealed that 40% of surveyed colonies (6 out of 15) entirely lacked male nymphs, indicating that such conditions may occur with non-negligible frequency in the wild. These findings suggest that worker-derived males gain rare but functional reproductive opportunities when typical male reproductives are absent, thereby maintaining their reproductive capacity over evolutionary timescales. This study provides important insight into the mechanisms that preserve reproductive totipotency in eusocial workers and underscores the value of examining reproductive roles in natural contexts to better understand the evolution of permanent sterility and true superorganismality.