Indirect development with an intermediate larva exists in all major animal lineages1, which makes larvae central to most scenarios 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 chromosome-scale genome sequencing in the annelid Owenia fusiformis with 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 of O. fusiformis but starts after gastrulation in the non-feeding larva with gradual metamorphosis of Capitella teleta and the direct developing embryo of Dimorphilus gyrociliatus. Accordingly, the embryos of O. fusiformis develop first into an enlarged anterior domain 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 temporal decoupling of head and trunk formation, as maximally observed in head larvae, facilitated larval evolution in Bilateria. This diverges from prevailing scenarios that propose either co-option9,10 or innovation11 of gene regulatory programmes to explain larva and adult origins.

Our understanding of the mechanisms that modulate gene expression in animals is strongly biased by studying a handful of model species that mainly belong to three groups: Insecta, Nematoda and Vertebrata. However, over half of the animal phyla belong to Spiralia, a morphologically and ecologically diverse animal clade with many species of economic and biomedical importance. Therefore, investigating genome regulation in this group is central to uncovering ancestral and derived features in genome functioning in animals, which can also be of significant societal impact. Here, we focus on five aspects of gene expression regulation to review our current knowledge of functional genomics in Spiralia. Although some fields, such as single-cell transcriptomics, are becoming more common, the study of chromatin accessibility, DNA methylation, histone post-translational modifications and genome architecture are still in their infancy. Recent efforts to generate chromosome-scale reference genome assemblies for greater species diversity and optimise state-of-the-art approaches for emerging spiralian research systems will address the existing knowledge gaps in functional genomics in this animal group.