The radial expression of dorsal-ventral patterning genes in placozoans,Trichoplax adhaerens,argues for an oral-aboral axis

Abstract

The placozoans are a morphologically simplistic group of marine animals found globally in tropical and subtropical environments. They consist of a single named species, Trichoplax adhaerens and have roughly six morphologically distinct cell types. With a sequenced genome, a limited number of cell-types and a simple flattened morphology, Trichoplax is an ideal model organism to understand cellular dynamics and tissue patterning in the first animals. Using new approaches for identification of gene expression patterns this research looks at the relationship of Chordin/TgfB signaling and the axial patterning system of Placozoa. Our results suggest that placozoans have an oral-aboral axis similar to cnidarians and that the parahoxozoan ancestor (common ancestor of Placozoa and Cnidaria) was likely radially symmetric.

Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias

“…However, if validated, this relationship must continue to raise questions on the homology of certain traits across non-bilaterians. Many workers, citing the incompletely known development ( Eitel et al, 2011 ; Pearse and Voigt, 2007 ) and relatively bilaterian-like gene content of placozoans ( Srivastava et al, 2008 ; Eitel, 2017 ), presume that these organisms must have a still-unobserved, more typical development and life cycle ( DuBuc et al, 2018 ), or else are merely oddities that have experienced wholesale secondary simplification, having scant significance to any evolutionary path outside their own. Indeed, it is tempting to interpret this new phylogenetic position as further bolstering such hypotheses, as much work on cnidarian models in the evo-devo paradigm is predicated on the notion that cnidarians and bilaterians share, more or less, many homologous morphological features, viz.…”

“…Indeed, it is tempting to interpret this new phylogenetic position as further bolstering such hypotheses, as much work on cnidarian models in the evo-devo paradigm is predicated on the notion that cnidarians and bilaterians share, more or less, many homologous morphological features, viz. axial organization ( Genikhovich and Technau, 2017 ; DuBuc et al, 2018 ), nervous systems ( Liebeskind et al, 2017 ; Moroz and Kohn, 2016 ; Kelava et al, 2015 ; Kristan, 2016 ; Arendt et al, 2016 ), basement-membrane lined epithelia ( Fidler et al, 2017 ; Leys and Riesgo, 2012 ), musculature ( Steinmetz et al, 2012 ), embryonic germ-layer organisation ( Steinmetz et al, 2017 ), and internal digestion ( Presnell et al, 2016 ; Putnam et al, 2007 ; Hejnol and Martindale, 2008 ; Martindale and Hejnol, 2009 ). While we do not argue, as some have done ( Schierwater, 2005 ; Syed and Schierwater, 2002 ), that placozoans resemble hypothetical metazoan ancestors, we hesitate to dismiss them a priori as irrelevant to understanding early bilaterian evolution in particular: although apparently simpler and less diverse, placozoans nonetheless have equal status to cnidarians as an immediate extant outgroup.…”

“…While we do not argue, as some have done ( Schierwater, 2005 ; Syed and Schierwater, 2002 ), that placozoans resemble hypothetical metazoan ancestors, we hesitate to dismiss them a priori as irrelevant to understanding early bilaterian evolution in particular: although apparently simpler and less diverse, placozoans nonetheless have equal status to cnidarians as an immediate extant outgroup. Rather, we see value in testing assumed hypotheses of homology, character by character, by extending pairwise comparisons between bilaterians and cnidarians to include placozoans, an agenda which demands reducing the large disparity in embryological, physiological, and molecular genetic knowledge between these taxa, towards which recent progress has been made using both established methods such as in situ hybridization ( DuBuc et al, 2018 ) and image analysis ( Varoqueaux, 2018 ), as well as new technologies such as single-cell RNA-seq ( Sebé-Pedrós, 2018a ; Sebé-Pedrós et al, 2018b ). Conversely, we emphasize another implication of this phylogeny: characters that can be validated as homologous at any level between Bilateria and Cnidaria must have originated earlier in animal evolution than previously appreciated, and should either cryptically occur in modern placozoans or else have been lost at some point in their ancestry.…”

The significance of sponges for comparative studies of developmental evolution

“…Some ctenophores can transiently form both a mouth and an anus, which seal through unknown mechanisms when not in use (Tamm, n.d.; Tamm & Tamm, ; Tamm, ). Placozoans are asymmetrical animals with oral/aboral patterning, but lack both a mouth and anus (DuBuc, Bobkov, Ryan, & Martindale, n.d.) and instead digest food externally, rather than in a gut (Fortunato & Aktipis, ).…”

Symmetry Transformations in Metazoan Evolution and Development

“…The ancestral metazoan complexity is deduced from the high degree of conservation of the gene family complements in contemporary animals [35]. This complexity is reflected by the presence of almost full gene family complement, such as the major toolkit genes Wnt, and in modern representatives of the earliest branching lineages, such as sponges, Trichoplax, and cnidarians [13,[51][52][53][54]. These data supported the proposal that ancient metazoans in the pre-Cambrian were already genetically complex, with most of the modern gene families and genomic organization already present [35].…”