Genomics, evolution and development of amphioxus and tunicates: The Goldilocks principle

Authors

  • Linda Z. Holland

    Corresponding author
    1. Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093-0202, USA
    • Correspondence to: Linda Z. Holland, Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0202 USA.

      E-mail: lzholland@ucsd.edu

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ABSTRACT

Morphological comparisons among extant animals have long been used to infer their long-extinct ancestors for which the fossil record is poor or non-existent. For evolution of the vertebrates, the comparison has typically involved amphioxus and vertebrates. Both groups are evolving relatively slowly, and their genomes share a high level of synteny. Both vertebrates and amphioxus have regulative development in which cell fates become fixed only gradually during embryogenesis. Thus, their development fits a modified hourglass model in which constraints are greatest at the phylotypic stage (i.e., the late neurula/early larva), but are somewhat greater on earlier development than on later development. In contrast, the third group of chordates, the tunicates, which are sister group to vertebrates, are evolving rapidly. Constraints on evolution of tunicate genomes are relaxed, and they have discarded key developmental genes and organized much of their coding sequences into operons, which are transcribed as a single mRNA that undergoes trans-splicing. This contrasts with vertebrates and amphioxus, whose genomes are not organized into operons. Concomitantly, tunicates have switched to determinant development with very early fixation of cell fates. Thus, tunicate development more closely fits a progressive divergence model (shaped more like a wine glass than an hourglass) in which the constraints on the zygote and very early development are greatest. This model can help explain why tunicate body plans are so very diverse. The relaxed constraints on development after early cleavage stages are correlated with relaxed constraints on genome evolution. The question remains: which came first? J. Exp. Zool. (Mol. Dev. Evol.) 324B: 342–352, 2015. © 2014 Wiley Periodicals, Inc.

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