Annelid functional genomics reveal the origins of bilaterian life cycles

Indirect development with an intermediate larva exists in all major animal lineages¹, making larvae central to most scenarios of animal evolution^2-12. Yet how larvae evolved remains disputed. Here we show that temporal shifts (i.e., heterochronies) in trunk formation underpin the diversification of larvae and bilaterian life cycles. Combining chromosome-scale genome sequencing in the slow-evolving annelidOwenia fusiformis¹³with transcriptomic and epigenomic profiling during the life cycles of this and two other annelids, we found that trunk development is deferred to pre-metamorphic stages in the feeding larva ofO. fusiformis, but starts after gastrulation in the non-feeding larva with gradual metamorphosis ofCapitella teletaand the direct developing embryo ofDimorphilus gyrociliatus. Accordingly, the embryos ofO. fusiformisdevelop first into an enlarged anterior domain that forms larval tissues and the adult head. Notably, this also occurs in the so-called “head larvae” of other bilaterians^14,15, with whomO. fusiformislarva shows extensive transcriptomic similarities. Together, our findings suggest that the temporal decoupling of head and trunk formation, as maximally observed in “head larvae”, allowed larval evolution in Bilateria, thus diverging from prevailing scenarios that propose either co-option^10,11or innovation¹²of gene regulatory programmes to explain larva and adult origins.