Preadaptation for asexual queen succession: queen tychoparthenogenesis produces neotenic queens in the termite Reticulitermes okinawanus

Social insects have evolved diverse breeding systems. In the termite species Reticulitermes speratus, queens produce their neotenic replacements parthenogenetically while producing other colony members sexually. This asexual queen succession (AQS) system enables the colony to undergo queen succession and increase the number of queens while avoiding king-daughter inbreeding, which must otherwise result in loss of genetic diversity in the workforce. The evolution of this sophisticated breeding system requires both parthenogenetic ability and parthenogens' developmental priority to become neotenic queens. However, the evolutionary process of these two components is unknown. In this study, we investigated the caste fate of the offspring produced by tychoparthenogenesis in a non-AQS termite species Reticulitermes okinawanus. The hatching rate of unfertilized eggs in R. okinawanus (0.97%) was much lower than that in the AQS species R. speratus (75%). Flow cytometry and genetic analyses were used to demonstrate that R. okinawanus tychoparthenogenesis produced diploid homozygous females. One-third of the daughters from unfertilized eggs developed into neotenics, while no sexually produced daughters differentiated into neotenics. These results suggest that parthenogenetic daughters have the developmental propensity to become neotenic queens prior to the inception of AQS.