Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction

Males and females are in conflict over genetic transmission in the evolution of parthenogenesis, because it enhances female reproductive output but deprives the males’ genetic contribution. For males, any trait that coerces females into sexual reproduction should increase their fitness. However, in the termite Reticulitermes speratus , queens produce their replacements (neotenic queens) parthenogenetically while using normal sexual reproduction to produce other colony members. Here, we show that termite queens produce parthenogenetic offspring in the presence of kings by closing the micropyles (sperm gates; i.e., openings for sperm entry) of their eggs. Our field survey showed that termite eggs show large variation in numbers of micropyles, with some having none. Microsatellite analysis showed that embryos of micropyleless eggs develop parthenogenetically, whereas those of eggs with micropyles are fertilized and develop sexually. Surveys of eggs among queens of different age groups showed that queens begin to lay micropyleless eggs when they are older and thus, need to produce their replacements parthenogenetically. In addition, we found clear seasonality in new neotenic queen differentiation and micropyleless egg production. This micropyle-dependent parthenogenesis is the first identification, to our knowledge, of the mechanism through which females control egg fertilization over time in diploid animals, implying a novel route of the evolution of parthenogenesis in favor of female interests without interference from males. Significance To clarify the evolution of parthenogenesis, given the potential sexual conflict over genetic transmission, identifying the mechanism regulating egg fertilization in females is essential. In the termite Reticulitermes speratus , queens produce their replacements (neotenic queens) parthenogenetically but use sexual reproduction to produce other colony members. We discovered that queens of the termite close micropyles (openings for sperm entry) of their eggs to produce parthenogenetic offspring in the presence of kings. Furthermore, we found that queens control the proportion of micropyleless eggs by regulating of the number of micropyles over time. This study describes a novel route of the evolution of parthenogenesis in favor of females’ interests without interference from males.