Lombricomposta

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Developmental Biology 312 (2007) 545 – 559 www.elsevier.com/developmentalbiology

The tardigrade Hypsibius dujardini, a new model for studying the evolution of development
Willow N. Gabriel a , Robert McNuff b , Sapna K. Patel a , T. Ryan Gregory c , William R. Jeck a , Corbin D. Jones a , Bob Goldstein a,⁎
a

Biology Department, University ofNorth Carolina at Chapel Hill, Chapel Hill, NC 27599, USA b Sciento, 61 Bury Old Road, Whitefield, Manchester, M45 6TB, England, UK c Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1 Received for publication 3 July 2007; revised 12 September 2007; accepted 28 September 2007 Available online 6 October 2007

Abstract Studying development in diverse taxa canaddress a central issue in evolutionary biology: how morphological diversity arises through the evolution of developmental mechanisms. Two of the best-studied developmental model organisms, the arthropod Drosophila and the nematode Caenorhabditis elegans, have been found to belong to a single protostome superclade, the Ecdysozoa. This finding suggests that a closely related ecdysozoan phylum couldserve as a valuable model for studying how developmental mechanisms evolve in ways that can produce diverse body plans. Tardigrades, also called water bears, make up a phylum of microscopic ecdysozoan animals. Tardigrades share many characteristics with C. elegans and Drosophila that could make them useful laboratory models, but long-term culturing of tardigrades historically has been a challenge,and there have been few studies of tardigrade development. Here, we show that the tardigrade Hypsibius dujardini can be cultured continuously for decades and can be cryopreserved. We report that H. dujardini has a compact genome, a little smaller than that of C. elegans or Drosophila, and that sequence evolution has occurred at a typical rate. H. dujardini has a short generation time, 13–14 daysat room temperature. We have found that the embryos of H. dujardini have a stereotyped cleavage pattern with asymmetric cell divisions, nuclear migrations, and cell migrations occurring in reproducible patterns. We present a cell lineage of the early embryo and an embryonic staging series. We expect that these data can serve as a platform for using H. dujardini as a model for studying the evolutionof developmental mechanisms. © 2007 Elsevier Inc. All rights reserved.
Keywords: Development; Evolution; Ecdysozoa; Tardigrade; Lineage; Model system

Introduction Recent advances in molecular phylogenies suggest that two well-studied model organisms, Caenorhabditis elegans (a nematode) and Drosophila melanogaster (an arthropod), are more closely related to each other than previously expected(Aguinaldo et al., 1997; Giribet and Ribera, 1998; Peterson and Eernisse, 2001; Copley et al., 2004; Dopazo and Dopazo, 2005). Both phyla are members of the Ecdysozoa, one of the two protostome superclades. Other ecdysozoan phyla could be valuable models to study the evolution of development, since such phyla may maximize the chance to make use of both the
⁎ Corresponding author. Fax: +1 919 9621625. E-mail address: bobg@unc.edu (B. Goldstein). 0012-1606/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2007.09.055

vast biological information and the techniques that have been developed in C. elegans and Drosophila. The other ecdysozoans comprise several of the least-studied animal phyla—loriciferans, kinorhynchs, priapulids, nematomorphs,onychophorans, and tardigrades (Fig. 1). The current problem with using the non-model ecdysozoan phyla for such studies is that very little is known about development in any of these groups. There have been some studies of embryonic development (Hyman, 1951; Anderson, 1973; Hejnol and Schnabel, 2005) and a few studies of developmental gene expression in these organisms (Panganiban et al., 1997; de Rosa et...