Early evolution of symmetry and polarity in metazoan body plans

Abstract

The early diverging metazoan lineages have highly disparate adult body plan geometries, which can be characterised in terms of five major types of symmetry (asymmetrical, spherical, cylindrical, n-radial, bilateral). Patterns of evolutionary changes in symmetry types and the homology of body axes across lineages are discussed here by confronting evidence from comparative anatomy, phylogeny, genomics and evo-devo. The conventional scenario, postulating a graded complexification from asymmetry to radial and finally bilateral symmetry, is considered untenable. Cylindrical symmetry is likely to be the ancestral type from which derived all remaining types through multiple convergences. Recent proposals prompted by molecular data that the bilateral anatomies of many cnidarians and of the Bilateria are homologous are clearly not supported. The Hox-based patterning system operating along the antero-posterior axis of the Bilateria does not seem to predate their divergence with the Cnidaria, but intercellular signalling systems, notably the Wnt pathway, could have been involved in generating the main body axis in the last common ancestor of the Metazoa.

β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii

“…Such observations have led to speculation that the Wnt pathway plays a conserved role in regulating eumetazoan embryonic axial patterning by participating in the specification of the blastoporal side, which corresponds to the posterior region in bilaterians and the oral region of cnidarians (Niehrs, 2010;Petersen and Reddien, 2009). However, homology between anteroposterior axis of bilaterians and oral-aboral axis of cnidarians is still a subject of controversy (Manuel, 2009;Martindale and Hejnol, 2009;Niehrs, 2010;Ryan and Baxevanis, 2007).…”

“…The Wnt pathway regulates many aspects of metazoan embryonic development, such as germ layer specification, determination of embryonic polarity, binary cell fate decision through asymmetric cell division, anteroposterior axis patterning and posterior growth (Guder et al, 2006a;Kusserow et al, 2005;Manuel, 2009;Martin and Kimelman, 2009;Niehrs, 2010;Petersen and Reddien, 2009). The animal-vegetal axis is the primary polarity of the oocyte and is defined by the site of polar body formation at the animal pole during meiosis.…”

Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans

“…E lucidation of macroevolutionary transitions between animal body plans remains to be a major challenge in evolutionary biology [1][2][3][4] , additionally complicated by disputable branching order of metazoan lineages 5,6 . Several lines of evidence (morphology, molecular phylogenies, fossil record) suggest that the first multicellular animals had poriferan-grade body plans with choanoflagellate-like cells (choanocytes) used for water movement, food capture and digestion, but lacked key metazoan cell types, for example, nerves and muscles [7][8][9][10][11][12] .…”

A new paradigm for animal symmetry

“…It also has to be said that the symmetry types which are practically possible in animals living in macroscopic three-dimensional space are also few in number [2], constituting a subset of all theoretically possible geometrical symmetries [3]. When an endless-or a great but finite-number of symmetry axes can be drawn through a body, then it is said to be spherically symmetrical (figure 1).…”