Reproductive constraint in the social aphid Ceratovacuna japonica: Sterility regulation in the soldier caste of a viviparous insect

Differentiation of the non-reproductive caste is a unique feature of eusocial insects. Apoptosis in oocytes plays a major role in constraining the reproductivity of the eusocial insects including bees, ants, and termites. However, the regulation of reproductive constraint in non-reproductives of primitively eusocial insects other than hymenopterans and blattodeans is almost unknown. Here, we investigated the soldier sterility in a hemipteran insect, the social aphid Ceratovacuna japonica. We compared the gonads of soldiers, that are completely sterile, with those of reproductives in their viviparous development. We found that soldiers possess a pair of ovaries and the same number of germaria as reproductives, but soldiers' ovarioles were small and lacking gastrulating embryos. Unlike in most model social insects, the staining of cleaved Caspase-3 showed apoptosis in the maternal nutritive cells, rather in the oocyte, of soldier ovaries. In addition, the ubiquitous C. japonica vasa1 and piwi2a expression indicates the developmental failure of embryos in soldier ovaries. The absence of posterior nos1, an insect posterior determinant, indicates deficient posterior patterning in soldier ovarioles. Our findings suggest a different mode of reproductive constraint, which regulates both oogenesis and embryogenesis in a viviparous insect ovary. This is the first report of the reproductive constraint in a viviparous social insect at the molecular level.

Automated summary

Differentiation of the non-reproductive caste is a unique feature of eusocial insects, and apoptosis in oocytes plays a major role in constraining their reproductivity. This study investigated the soldier sterility in a hemipteran insect, the social aphid Ceratovacuna japonica, and found that soldiers possess ovaries and germaria but their ovarioles are small and lacking gastrulating embryos. The study also revealed apoptosis in the maternal nutritive cells of soldier ovaries and developmental failure of embryos.