The genome of the jellyfish Aurelia and the evolution of animal complexity
David A. Gold, Takeo Katsuki, Yang Li, Xifeng Yan, Michael Regulski, David Ibberson, Thomas Holstein, Robert E. Steele, David K. Jacobs & Ralph J. Greenspan
Nature Ecology & Evolution volume 3, pages96–104 (2019)
Cnidarian relationships, life cycles and sensory structures
Abstract
We present the genome of the moon jellyfish Aurelia, a genome from a cnidarian with a medusa life stage. Our analyses suggest that gene gain and loss in Aurelia is comparable to what has been found in its morphologically simpler relatives—the anthozoan corals and sea anemones. RNA sequencing analysis does not support the hypothesis that taxonomically restricted (orphan) genes play an oversized role in the development of the medusa stage. Instead, genes broadly conserved across animals and eukaryotes play comparable roles throughout the life cycle. All life stages of Aurelia are significantly enriched in the expression of genes that are hypothesized to interact in protein networks found in bilaterian animals. Collectively, our results suggest that increased life cycle complexity in Aurelia does not correlate with an increased number of genes. This leads to two possible evolutionary scenarios: either medusozoans evolved their complex medusa life stage (with concomitant shifts into new ecological niches) primarily by re-working genetic pathways already present in the last common ancestor of cnidarians, or the earliest cnidarians had a medusa life stage, which was subsequently lost in the anthozoans. While we favour the earlier hypothesis, the latter is consistent with growing evidence that many of the earliest animals were more physically complex than previously hypothesized.
Acknowledgements
We thank K. Kosik and N. Nakanishi for their insights during the development of this project; R. Warren for his advice on genome assembly strategy; V. Levesque and the Birch Aquarium at Scripps for providing Aurelia strains; and S. Johnson, D. Le, D. Lam, and A. Hsu for technical assistance. D.A.G. gratefully acknowledges funding from a National Institutes of Health Training Grant in Genomic Analysis and Interpretation (T32HG002536) and a Cordes Postdoctoral Fellowship from the Division of Biology and Biological Engineering at Caltech. This work was also supported by grants from the W.M. Keck Foundation (R.J.G.), the Gordon and Betty Moore Foundation (R.J.G.), the DFG (T.H.), a fellowship from the Uehara Memorial Foundation (T.K.) and the NASA Astrobiology Institute–Foundations of Complex Life: Evolution, Preservation and Detection on Earth and Beyond (D.K.J.).
Author information
Author notes
These authors contributed equally: D. A. Gold, T. Katsuki, R. J. Greenspan.
Affiliations
Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
David A. Gold
Department of Earth and Planetary Sciences, University of California Davis, Davis, CA, USA
David A. Gold
Kavli Institute for Brain and Mind, University of California San Diego, La Jolla, CA, USA
Takeo Katsuki & Ralph J. Greenspan
Department of Computer Science, University of California Santa Barbara, Santa Barbara, CA, USA
Yang Li & Xifeng Yan
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
Michael Regulski
Deep Sequencing Core Facility, Cell Networks, Heidelberg University, Heidelberg, Germany
David Ibberson
Department of Molecular Evolution and Genomics, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
Thomas Holstein
Department of Biological Chemistry and Developmental Biology Center, University of California Irvine, Irvine, CA, USA
Robert E. Steele
Department of Ecology and Evolution, University of California Los Angeles, Los Angeles, CA, USA
David K. Jacobs
Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA
Ralph J. Greenspan
Department of Cognitive Science, University of California San Diego, La Jolla, CA, USA
Ralph J. Greenspan
Contributions
R.J.G. and T.K. sequenced and assembled the genome with input from R.E.S. M.R. contributed 100-bp paired-end reads, and D.I. and T.H. provided mate-pair reads with 4-kbp inserts. X.Y. and Y.L. worked on the initial error correction of PacBio reads. D.K.J. and D.A.G. oversaw transcriptome sequencing and assembly. D.A.G. performed downstream analyses of genome annotation with input from T.K., R.J.G., R.E.S. and D.K.J. D.A.G. designed the figures and drafted the manuscript. All authors reviewed and approved the final paper.
Competing interests
The authors declare no competing interests.
Corresponding authors
Correspondence to David A. Gold or Takeo Katsuki or Ralph J. Greenspan.
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