Annelid functional genomics reveal the origins of bilaterian life cycles

Francisco M. Martín-Zamora, Yan Liang, Kero Guynes, Allan M. Carrillo-Baltodano, Billie E. Davies, Rory D. Donnellan, Yongkai Tan, Giacomo Moggioli, Océane Seudre, Martin Tran, Kate Mortimer, Nicholas M. Luscombe, Andreas Hejnol, Ferdinand Marlétaz () and José M. Martín-Durán ()
Additional contact information
Francisco M. Martín-Zamora: Queen Mary University of London
Yan Liang: Queen Mary University of London
Kero Guynes: Queen Mary University of London
Allan M. Carrillo-Baltodano: Queen Mary University of London
Billie E. Davies: Queen Mary University of London
Rory D. Donnellan: Queen Mary University of London
Yongkai Tan: Okinawa Institute of Science and Technology Graduate University
Giacomo Moggioli: Queen Mary University of London
Océane Seudre: Queen Mary University of London
Martin Tran: Queen Mary University of London
Kate Mortimer: Amgueddfa Cymru–Museum Wales
Nicholas M. Luscombe: Okinawa Institute of Science and Technology Graduate University
Andreas Hejnol: University of Bergen
Ferdinand Marlétaz: University College London
José M. Martín-Durán: Queen Mary University of London

Nature, 2023, vol. 615, issue 7950, 105-110

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41586-022-05636-7

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