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On the Evolution of Bilaterality Grigory Genikhovich* and Ulrich Technau*

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On the Evolution of Bilaterality Grigory Genikhovich* and Ulrich Technau* © 2017. Published by The Company of Biologists Ltd | Development (2017) 144, 3392-3404 doi:10.1242/dev.141507 HYPOTHESIS On the evolution of bilaterality Grigory Genikhovich* and Ulrich Technau* ABSTRACT group of Bilateria (Cannon et al., 2016; Hejnol et al., 2009; Moroz Bilaterality – the possession of two orthogonal body axes – is the et al., 2014; Philippe et al., 2011; Pisani et al., 2015; Whelan et al., name-giving trait of all bilaterian animals. These body axes are 2015), are of particular interest. Cnidarian morphology does not established during early embryogenesis and serve as a three- permit one to distinguish a dorsal and a ventral side, and no obvious dimensional coordinate system that provides crucial spatial cues for left-right asymmetry exists. However, while four cnidarian classes developing cells, tissues, organs and appendages. The emergence (Hydrozoa, Scyphozoa, Cubozoa and Staurozoa; uniting various of bilaterality was a major evolutionary transition, as it allowed animals jellyfish and hydroids) are combined into the Medusozoa, which to evolve more complex body plans. Therefore, how bilaterality consist of animals with radial symmetry, members of the fifth evolved and whether it evolved once or several times independently cnidarian class Anthozoa (encompassing hard corals, sea is a fundamental issue in evolutionary developmental biology. Recent anemones, soft corals and sea pens) (Collins et al., 2006) are findings from non-bilaterian animals, in particular from Cnidaria, the bilaterally symmetric (Fig. 1); in addition to the oral-aboral axis that sister group to Bilateria, have shed new light into the evolutionary is common to all Cnidaria, anthozoans have a second, so-called ‘ ’ origin of bilaterality. Here, we compare the molecular control of body directive , axis running along the slit-like pharynx orthogonally to axes in radially and bilaterally symmetric cnidarians and bilaterians, the oral-aboral axis. It is therefore particularly interesting to examine identify the minimal set of traits common for Bilateria, and evaluate whether the bilaterality of Anthozoa and Bilateria was inherited whether bilaterality arose once or more than once during evolution. from a bilaterally symmetric common ancestor and then lost in the radially symmetric Medusozoa, or whether it evolved convergently KEY WORDS: Bilateria, Cnidaria, Bilateral symmetry, Body axes (Fig. 1). Furthermore, in the case of a homologous origin, we wish to know which of the cnidarian body axes correspond to the Introduction anterior-posterior and to the D-V body axis of Bilateria. In this Most animals belong to Bilateria (see Glossary, Box 1), a group review, we summarize and compare the molecular regulation of encompassing organisms with three germ layers (ectoderm, body axes in Bilateria and in cnidarians, as well as in Porifera and endoderm and mesoderm) and two body axes, i.e. an anterior- Ctenophora, and evaluate different scenarios of how bilaterality may posterior axis and a dorsal-ventral (D-V) axis. Body axes can be have emerged. In order to do so, we first define the sets of features thought of as systems of molecular coordinates (Niehrs, 2010), that are typical for the body axes of bilaterians, cnidarians and the allowing different parts of the body to develop differently. For evolutionary outgroups to the bilaterian-cnidarian clade: the example, the central nervous system develops at the dorsal side of ctenophores and sponges. the vertebrate body, but ventrally in insects and many other animals. The anterior end is usually characterized by a concentration of Reconstructing the bilaterian ancestor sensory organs, such as eyes and the olfactory system. Bilaterality Axis formation has been studied most thoroughly in several also favours the formation of left-right asymmetry in many animals, vertebrates (i.e. mouse, zebrafish, Xenopus) and especially in the including vertebrates. However, among the non-bilaterian Metazoa fruit fly Drosophila, which became the textbook example. In (see Glossary, Box 1), other types of symmetry exist (Fig. 1). For Drosophila, maternally established gradients of the transcription example, sponges (Porifera), although missing a clear body factor Bicoid and the RNA-binding protein Nanos define the symmetry in their modular, sessile adult state, have an obvious anterior and posterior ends, and activate a complex cascade of radial symmetry as larvae. Comb jellies (Ctenophora) are bi-radially gene regulatory interactions that eventually lead to segmentation symmetric, with an oral-aboral axis and two other planes of and regional specification of the anterior-posterior axis (Gilbert, symmetry, one going through the bases of the tentacles and the other 2010). However, in other arthropods, such as beetles, centipedes through the slit-like mouth. Placozoans are irregularly shaped, and spiders, as well as in vertebrates, segmentation involves a crawling animals that exhibit a dorsal and ventral surface, although Hairy/Notch/Delta-dependent clock-like oscillation mechanism, how these surfaces arise is unclear as placozoan embryogenesis is which is initiated and controlled by a gradient of Wnt signalling unknown. These various types of symmetry and body axes raise the (and, in the case of vertebrates, also by FGF signalling) from the question of how and when bilaterality – a trait that likely contributed posterior end (Chipman and Akam, 2008; El-Sherif et al., 2012; to the diversification of body plans (see Box 2) – might have arisen. Gomez et al., 2008; Janssen et al., 2010; McGregor et al., 2008; In the debate about the evolutionary origin of bilaterality, Schönauer et al., 2016; Stollewerk et al., 2003). Strikingly, the Cnidaria, which are robustly recovered as the phylogenetic sister crucial developmental regulator bicoid turned out to be an evolutionary innovation within Diptera (the insect order that includes Drosophila) that arose through duplication and Department for Molecular Evolution and Development, Centre of Organismal Systems Biology, University of Vienna, Althanstraße 14, A-1090 Vienna, Austria. divergence of the hox3 gene homologue zerknüllt (Stauber et al., 2002). This clearly shows how plastic the crucial aspects *Authors for correspondence ([email protected]; ulrich.technau@ of the regulation of animal development can be, and also univie.ac.at) highlights the importance of broad phylogenetic sampling when G.G., 0000-0003-4864-7770; U.T., 0000-0003-4472-8258 defining ancestral molecular features. DEVELOPMENT 3392 HYPOTHESIS Development (2017) 144, 3392-3404 doi:10.1242/dev.141507 D Box 1. Glossary Chordata Bilateria Acoela. A group of animals with a single gut opening previously thought D to be members of flatworms, but now usually placed within the earliest Ambulacraria A V branching bilaterian lineage Xenacoelomorpha. Spiralia P O Ambulacraria. Besides chordates, one of the two major clades of P Deuterostomia. Ambulacraria includes echinoderms (sea urchins, Ecdysozoa A starfish, etc.) and hemichordates. In contrast to chordates, Directive Xenacoelomorpha A ambulacrarians do not have a centralized nervous system and, similar to non-deuterostome Bilateria, possess a ventral BMP signalling Anthozoa minimum. Staurozoa Amphistomy. The mode of gastrulation in which the lateral lips of the O Cnidaria blastopore fuse in a slit-like fashion leaving two openings: an anterior Cubozoa mouth and a posterior anus connected by a U-shaped gut. DS Bilateria. The phylogenetic group of bilaterally symmetric animals, Scyphozoa VS consisting of three germ layers. Bilateria are subdivided into Hydrozoa Xenacoelomorpha, Deuterostomia and Protostomia. A Chordata. The second major clade of Deuterostomia, including Placozoa O cephalochordates (amphioxus), tunicates (ascidians, larvaceans, etc.) and vertebrates. Ctenophora Deuterostomia. An animal group consisting of Ambulacraria and Veg Chordata. The name comes from the fact that their mouth forms Porifera An separately from the blastopore. Ecdysozoa. An animal clade uniting moulting animals (nematodes, Key priapulids, arthopods, etc.). P Protostomia D Deuterostomia GLWamide-positive neurons. Neurons expressing neuropeptides Scenario 1: Gain of bilaterality Loss of bilaterality carrying GLWamide on the C terminus. Scenario 2: Independent gains of bilaterality Lophotrochozoa. An animal clade uniting groups with trochophore-like larvae (molluscs, annelids, ribbon worms, etc.) and lophophorate animals (bryozoans, brachiopods, etc.). Currently considered as a Fig. 1. The distribution of different body symmetries among animals. subclade within Spiralia, which include also Gnathifera Alternative scenarios that can explain the emergence of bilaterality are (gnathostomulids, rotifers, etc.) and Rouphozoa (flatworms, depicted. An-Veg, animal-vegetal; DS-VS, dorsal surface-ventral surface; O-A, gastrotrichs), and uniting animals with spiral cleavage. oral-aboral; A-P, anterior-posterior; D-V, dorsal-ventral. Mesenteries. Endodermal folds of anthozoans harbouring longitudinal muscles and gonads. genes nk2.2, nk6, pax6 and msx, which pattern the ventral nerve Metazoa. The clade uniting all animal phyla. Planula. A type of diploblastic ciliated larva typical for all cnidarian cord of flies and worms, and the dorsal neural tube of vertebrates clades. (Arendt et al., 2008; Denes et al., 2007; Tessmar-Raible et al., Primary polyp. A developmental stage following metamorphosis of the 2007). cnidarian planula. A Nematostella primary polyp has four tentacles. As it As
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