Annelid functional genomics reveal the origins of bilaterian life cycles

Indirect development with an intermediate larva exists in all major animal lineages1, which makes larvae central to mostscenarios of animal evolution2-11. Yet how larvae evolved remains disputed. Here we show that temporal shifts (that is,heterochronies) in trunk formation underpin the diversification of larvae and bilaterian life cycles. We performed chromosomescalegenome sequencing in the annelid Owenia fusiformis with transcriptomic and epigenomic profiling during the life cycles ofthis and two other annelids. We found that trunk development is deferred to pre-metamorphic stages in the feeding larva of O.fusiformis but starts after gastrulation in the non-feeding larva with gradual metamorphosis of Capitella teleta and the directdeveloping embryo of Dimorphilus gyrociliatus. Accordingly, the embryos of O. fusiformis develop first into an enlarged anteriordomain that forms larval tissues and the adult head12. Notably, this also occurs in the so-called 'head larvae' of other bilaterians13-17, with which the O. fusiformis larva shows extensive transcriptomic similarities. Together, our findings suggest that the temporaldecoupling of head and trunk formation, as maximally observed in head larvae, facilitated larval evolution in Bilateria. Thisdiverges from prevailing scenarios that propose either co-option9,10 or innovation11 of gene regulatory programmes to explainlarva and adult origins.