Offspring chemical control of adult reproductive transitions in a social insect

Abstract

Parental care enhances offspring survival and growth but often entails a trade-off in which caregivers temporarily suppress their own reproduction to invest in existing young. In vertebrates, these parental reproductive cycles are controlled by offspring-derived cues that reduce or suppress parental fertility. While many insects display obligate parental care, the role of offspring cues in regulating adult reproduction remains unresolved outside advanced eusocial taxa, where reproductive cycles have largely been lost. Here, we investigate reproductive cycles in the clonal raider ant Ooceraea biroi, in which totipotent females alternate between caring for larvae and laying eggs. Using custom behavioral assays, we show that larvae inhibit adult reproduction without physical contact, implicating volatile cues. Chemical analyses identified a previously undescribed larva-specific compound, methyl 3-ethyl-2-hydroxy-4-methylpentanoate (MEHMP), which is absent from other developmental stages and ant species. Exposure to synthetic MEHMP recapitulated the inhibitory effect of larval volatiles, confirming its role as a pheromone that suppresses adult egg laying. To our knowledge, this is the first brood pheromone described in ants. By providing a direct chemical link between offspring presence and parental reproductive suppression, our findings underscore the central role of offspring signals in mediating parental reproductive investment across animals that care for their young. Significance StatementParental care enhances offspring survival but induces profound physiological changes in caregivers. A common feature across animals is that adults temporarily suppress their own reproduction while caring for the young. The offspring cues enforcing these cycles remain poorly understood, especially in insects. Using the clonal raider ant Ooceraea biroi, in which all females alternate between reproduction and brood care, we identify a larval pheromone that suppresses adult egg laying. This pheromone is a previously undescribed volatile chemical compound, and exposure to its synthetic version mimics the full biological effect of larvae volatiles. By providing a direct link between offspring presence and adult reproductive suppression, our work highlights how offspring can chemically control the reproduction of their caregivers.