External morphogenesis of the tardigradeHypsibius dujardinias revealed by scanning electron microscopy

Abstract

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.

Expression of NK genes that are not part of the NK cluster in the onychophoran Euperipatoides rowelli (Peripatopsidae)

“…If so, one would expect a similar pattern of expression in the lobopods of onychophorans – unjointed, tube-like limbs that are also found in tardigrades (water bears) (e.g., refs [118, 119]) and Cambrian lobopodians (e.g. ref.…”

The Emergence of the TardigradeHypsibius exemplarisas a Model System

“…Most of the recent developmental studies on tardigrades have used H. exemplaris strain Z151 from Sciento Gross and Mayer 2015;Hyra et al 2016a,b;Smith et al 2016;Gross et al 2017). Studies that used H. exemplaris strain Z151 prior to the 2018 species disambiguation from H. dujardini (Gasiorek et al 2018) generally referred to the species as H. dujardini, or as Hypsibius cf.…”

“…Studies that used H. exemplaris strain Z151 prior to the 2018 species disambiguation from H. dujardini (Gasiorek et al 2018) generally referred to the species as H. dujardini, or as Hypsibius cf. dujardini, and in many of these studies the strain was indicated as Z151 and/or sourced from Sciento Bavan et al 2009;Mali et al 2010;Cesari et al 2012;Beltrán-Pardo et al 2013;Horikawa et al 2013;Tenlen et al 2013;Smith and Jockusch 2014;Boothby et al 2015Boothby et al , 2017Gross and Mayer 2015;Kondo et al 2015;Arakawa et al 2016;Bemm et al 2016;Fernandez et al 2016;Hering et al 2016;Hyra et al 2016a,b;Kosztyła et al 2016;Koutsovoulos et al 2016;Levin et al 2016;Smith et al 2016Stec et al 2016;Erdmann et al 2017;Gross et al 2017Gross et al , 2018Vasanthan et al 2017;Yoshida et al 2017Yoshida et al , 2018Fadero et al 2018;Nelson 2018;Rost-Roszkowska et al 2018). One study using Thulinia stephaniae (Hejnol and Schnabel 2005) indicates some contrasting developmental features in a second tardigrade species.…”

“…Studies using this model and the other tardigrade species mentioned above have focused mostly on survival in extreme conditions in the laboratory (Guidetti et al 2011;Horikawa et al 2013;Beltrán-Pardo et al 2015;Fernandez et al 2016;Vasanthan et al 2017), identifying extremotolerance mechanisms (Kondo et al 2015;Hashimoto et al 2016;Boothby et al 2017), development and anatomy and the evolution of development and anatomy Mayer et al 2013;Smith and Jockusch 2014;Gross and Mayer 2015;Hyra et al 2016a,b;Smith et al 2016;Gross et al 2017), taxonomic methods and relationships (Rota-Stabelli et al 2010;Stec et al 2016), sequence comparisons with other species (Förster et al 2009;Mali et al 2010;Christie et al 2011;D'Haese et al 2011;Beltrán-Pardo et al 2013;Hering and Mayer 2014;Mayer et al 2015;Szitenberg et al 2016;Thiruketheeswaran et al 2017;Nelson 2018), and analyses of specific proteins (Bavan et al 2009;Hering et al 2016). Genomic studies are discussed in a section below.…”

A Hypothesis for the Composition of the Tardigrade Brain and its Implications for Panarthropod Brain Evolution

“…The relatively simple tardigrade brain may hold important clues regarding the transition from a cycloneuralian brain to a ganglionic brain in the panarthropod stem lineage. Unlike the brains of euarthropods and onychophorans, which are composed of multiple segmental ganglia (Scholtz and Edgecombe 2006;Strausfeld et al 2006a;Mayer et al 2010;Whitington and Mayer 2011;Martin and Mayer 2015), the tardigrade brain is composed of a single segmental ganglion (Hejnol and Schnabel 2005;Mayer et al 2013a;Gross and Mayer 2015;Smith et al 2016;Gross et al 2017; see Zantke et al 2008 andPersson et al 2012 for alternative views)-a condition that is thought to be plesiomorphic for Panarthropoda (reviewed in Strausfeld 2012; Smith and Goldstein 2017;Ortega-Hern andez et al 2017). Furthermore, Tardigrada is most likely the sister group of a Euarthropoda þ Onychophora clade (Campbell et al 2011;Rota-Stabelli et al 2013;Dunn et al 2014;Giribet 2016; for an alternative view, see Borner et al 2014 andLaumer et al 2015;reviewed in Edgecombe and Giribet, this volume).…”