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Annelid functional genomics reveal the origins of bilaterian life cycles

View ORCID ProfileYan Liang, View ORCID ProfileFrancisco M. Martín-Zamora, View ORCID ProfileKero Guynes, View ORCID ProfileAllan M. Carrillo-Baltodano, Yongkai Tan, Giacomo Moggioli, View ORCID ProfileOcéane Seudre, Martin Tran, View ORCID ProfileKate Mortimer, View ORCID ProfileNicholas M. Luscombe, View ORCID ProfileAndreas Hejnol, View ORCID ProfileFerdinand Marlétaz, View ORCID ProfileJosé M. Martín-Durán
doi: https://doi.org/10.1101/2022.02.05.479245
Yan Liang
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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Francisco M. Martín-Zamora
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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  • ORCID record for Francisco M. Martín-Zamora
Kero Guynes
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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Allan M. Carrillo-Baltodano
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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Yongkai Tan
2Genomics and Regulatory Systems Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
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Giacomo Moggioli
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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Océane Seudre
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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  • ORCID record for Océane Seudre
Martin Tran
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
3Department of Infectious Disease, Imperial College London, London, United Kingdom
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Kate Mortimer
4Department of Natural Sciences, Amgueddfa Cymru – National Museum Wales, Cardiff, United Kingdom
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Nicholas M. Luscombe
2Genomics and Regulatory Systems Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
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Andreas Hejnol
5Department of Biological Sciences, University of Bergen, Bergen, Norway
6Institute of Zoology and Evolutionary Research, Friedrich-Schiller-University Jena, Jena, Germany
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Ferdinand Marlétaz
7Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan
8Department of Genetics, Evolution and Environment, University College London, London, United Kingdom
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  • For correspondence: chema.martin@qmul.ac.uk f.marletaz@ucl.ac.uk
José M. Martín-Durán
1School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom
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  • ORCID record for José M. Martín-Durán
  • For correspondence: chema.martin@qmul.ac.uk f.marletaz@ucl.ac.uk
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ABSTRACT

Indirect development with an intermediate larva exists in all major animal lineages1, and thus larvae are central to most scenarios for animal evolution2–12. Yet how larvae evolved remains disputed. Here we show that changes in the timing of trunk formation underpin the diversification of larvae and bilaterian life cycles. Combining chromosome-scale genome sequencing with transcriptomic and epigenomic profiling in the slow-evolving oweniid Owenia fusiformis13, we found that different genes and genomic regulatory elements control the development of its feeding larva and adult stage. First, O. fusiformis embryos develop into an enlarged anterior domain that forms larval tissues and the adult head, as posterior growth and trunk patterning is deferred to pre-metamorphic stages. These traits also occur in the so-called “head larvae” of other bilaterians14,15, with whom O. fusiformis larva shows extensive transcriptomic similarities. Conversely, animals with non-feeding larvae and gradual metamorphoses, such as the annelid Capitella teleta, start trunk differentiation during embryogenesis, like direct developers. Together, our findings suggest that the ancestral temporal decoupling of head and trunk formation, as retained in extant “head larvae”, allowed larval evolution in Bilateria, questioning prevailing scenarios that propose either co-option10,11 or innovation12 of gene regulatory programmes to explain larva and adult origins.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/ChemaMD/OweniaGenome

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 06, 2022.
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Annelid functional genomics reveal the origins of bilaterian life cycles
Yan Liang, Francisco M. Martín-Zamora, Kero Guynes, Allan M. Carrillo-Baltodano, Yongkai Tan, Giacomo Moggioli, Océane Seudre, Martin Tran, Kate Mortimer, Nicholas M. Luscombe, Andreas Hejnol, Ferdinand Marlétaz, José M. Martín-Durán
bioRxiv 2022.02.05.479245; doi: https://doi.org/10.1101/2022.02.05.479245
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Annelid functional genomics reveal the origins of bilaterian life cycles
Yan Liang, Francisco M. Martín-Zamora, Kero Guynes, Allan M. Carrillo-Baltodano, Yongkai Tan, Giacomo Moggioli, Océane Seudre, Martin Tran, Kate Mortimer, Nicholas M. Luscombe, Andreas Hejnol, Ferdinand Marlétaz, José M. Martín-Durán
bioRxiv 2022.02.05.479245; doi: https://doi.org/10.1101/2022.02.05.479245

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