Faster and smaller: Heterochronic shift in gene expression leads to larval onset of spermatogenesis and miniaturized males

Heterochrony, a change in the timing of developmental events, is suggested as the prevailing evolutionary route to an underdeveloped or pedomorphic body plan. Many microscopic animal lineages (meiofauna) are hypothesized to descend from macroscopic ancestors, but direct evidence linking miniaturization to heterochronic shifts in development is scarce. Here, we investigate the molecular developmental basis of the dimorphic annelid Osedax japonicus , which has bone-eating macroscopic females and microscopic, pedomorphic males. We find that males start their sexual maturation extremely early, with testes already developing in the larval stage, and cease their somatic growth soon after metamorphosis. Heterochronic shifts in gene expression explain this male pedomorphosis through early onset of germline development, sexual determination, and maturation in concert with early offset of somatic growth. Our findings provide direct developmental evidence for how heterochrony can drive extreme miniaturization, shedding new light on the evolutionary origins of microscopic animal lineages.