External morphogenesis of the tardigrade Hypsibius dujardini as revealed by scanning electron microscopy.
Tardigrada, commonly called water bears, is a taxon of microscopic panarthropods with five-segmented bodies and four pairs of walking legs. Although tardigrades have been known to science for several centuries, questions remain regarding many aspects of their biology, such as embryogenesis. Herein, we used scanning electron microscopy to document the external changes that occur during embryonic development in the tardigrade Hypsibius dujardini (Eutardigrada, Parachela, Hypsibiidae). Our results show an accelerated development of external features, with approximately 30 hrs separating the point at which external structures first become recognizable and a fully formed embryo. All segments appear to arise simultaneously between ∼20 and 25 hrs of development, and no differences in the degree of development could be detected between the limb buds at any stage. Claws emerge shortly after the limb buds and are morphologically similar to those of adults. The origin of the claws is concurrent with that of the sclerotized parts of the mouth, suggesting that all cuticular structures arise simultaneously at ∼30 hrs. The mouth arises as an invagination in the terminal region of the head at ∼25 hrs, closes later in development, and opens again shortly before hatching. The anlagen of the peribuccal lobes arise as one dorsal and one ventral row, each consisting of three lobes, and later form a ring in the late embryo, whereas there is no indication of a labrum anlage at any point during development. Furthermore, we describe limited postembryonic development in the form of cuticular pores that are absent in juveniles but present in adults. This study represents the first scanning electron micrographs of tardigrade embryos, demonstrating the utility of this technique for studying embryogenesis in tardigrades. This work further adds an external morphological perspective to the developmental data already available for H. dujardini, facilitating future comparisons to related panarthropod taxa. J. Morphol. 278:563-573, 2017. © 2017 Wiley Periodicals, Inc.
Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34132, Kassel, Germany.
Vladimir
0000-0001-7422-9148
V
Gross
Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34132, Kassel, Germany.
Irene
I
Minich
Department of Zoology, Institute of Biology, University of Kassel, Heinrich-Plett-Straße 40, D-34132, Kassel, Germany.
Georg
G
Mayer
D000818:Animals; D004625:Embryo, Nonmammalian / Q000033:anatomy & histology / Q000648:ultrastructure; D047108:Embryonic Development; D005121:Extremities / Q000196:embryology; D008855:Microscopy, Electron, Scanning / Q000379:methods*; D009024:Morphogenesis; D058467:Tardigrada / Q000196:embryology* / Q000648:ultrastructure*
Ecdysozoa; Panarthropoda; arthropod evolution; direct development; embryology; scanning electron microscopy