Hermaphrodites have lower metabolic rates than gonochores

Hermaphroditism, where an individual can reproduce as both male and female, offers some clear reproductive advantages. Simultaneous hermaphroditism guarantees that every mature adult can mate with another – a particular advantage when opportunities to mate are scarce. Despite this potential benefit, hermaphroditism is relatively rare in animals. This paradox has long involved an energetics argument: hermaphrodites require more energy to fuel two reproductive roles instead of only one, which favours the evolution of separate sexes. However, this argument has never been tested. Here, we compare resting metabolic rates between hermaphrodites and gonochores across 536 species of marine invertebrates, spanning 11 phyla. Our analyses, which control for body size, environmental temperature, motility, and phylogeny, contradict predictions from classic theory: instead of requiring more energy than gonochores, hermaphrodites require ~27% less energy on average. These findings overturn a 150-year-old argument that hermaphroditism is rarer in animals because it is more costly, and highlight the need to reconsider the role of energetics in the evolution of sexual systems.