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The significance of sponges for comparative studies of developmental evolution

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Abstract Sponges, ctenophores, placozoans, and cnidarians have key evolutionary significance in that they bracket the time interval during which organized animal tissues were first assembled, fundamental cell types originated (e.g., neurons and myocytes), and developmental patterning mechanisms evolved. Sponges in particular have often been viewed as living surrogates for early animal ancestors, largely due to similarities between their feeding cells (choanocytes) with choanoflagellates, the unicellular/colony‐forming sister group to animals. Here, we evaluate these claims and highlight aspects of sponge biology with comparative value for understanding developmental evolution, irrespective of the purported antiquity of their body plan. Specifically, we argue that sponges strike a different balance between patterning and plasticity than other animals, and that environmental inputs may have prominence over genetically regulated developmental mechanisms. We then present a case study to illustrate how contractile epithelia in sponges can help unravel the complex ancestry of an ancient animal cell type, myocytes, which sponges lack. Sponges represent hundreds of millions of years of largely unexamined evolutionary experimentation within animals. Their phylogenetic placement lends them key significance for learning about the past, and their divergent biology challenges current views about the scope of animal cell and developmental biology. This article is characterized under: Comparative Development and Evolution > Evolutionary Novelties Comparative Development and Evolution > Body Plan Evolution
Competing hypotheses about the evolution of collar cells. Choanoflagellates resemble choanocytes, the feeding cells of sponges. (a) The traditional perspective is that the similarity between these cell types reflects their descent from a common ancestral cell type, and that detected differences between these cell types result from >600 million years ago of divergent evolution. (b) An alternative hypothesis is that the resemblance of choanoflagellates and choanocytes is superficial and reflects convergent evolution for efficient bacterivorous filter‐feeding by a collar cell. Collar‐like cells are present in non‐sponge animals, but have functions other than bacterivory
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A comparative framework for studies of early evolution in animals. (a) Lineages like sponges, ctenophores, placozoans, and cnidarians bracket the earliest periods of animal evolution, yet we have only begun to study their cell and developmental biology from a mechanistic perspective. These lineages comprise half (or more) of deep phylogenetic diversity within animals. (b) The anatomy of sponges diverges considerably from other animals. They are essentially epithelial organisms organized around a network of internal water canals. Water flows (arrows) in through incurrent canals (In), travels through choanocyte chambers (cc; highlighted in red) where bacteria (and other picoplankton) are phagocytosed by choanocytes, then leaves via excurrent canals (Exc) that lead to the exhalant siphon (the osculum; Osc). Migratory cells (Mig) are found in the interior, as are skeletal elements (spicules; Sp). The box (left) shows a higher magnification depiction of the primary sponge tissues including the exopinacoderm (outer layer; Exp), porocytes (specialized cells that regulate incurrent water flow; Pc), endopinacocytes (the inner epithelial lining; Enp), choanocytes of a choanocyte chamber, and archeocytes (migratory stem cells; Ac). (All images in panel a are from PhyloPic.org. Artistic credits: Sponge = Mali'o Kodis, photograph by Derek Keats (http://www.flickr.com/photos/dkeats/); Mnemiopsis = Mali'o Kodis, photograph by Aqua‐Photos (https://www.flickr.com/people/undervannsfotografen/); Xenopus = Sara Werning; Strongylocentrotus = Frank Förster (based on a picture by Jerry Kirkhart; modified by T. Michael Keesey); Trichoplax = Oliver Voigt; all listed images are available for use under the following license: https://creativecommons.org/licenses/by‐sa/3.0/legalcode
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Actin organization in the sponge Ephydatia muelleri and the cnidarian Nematostella vectensis. (a) Whole‐mount F‐actin staining in an E. muelleri juvenile. White overlay marks the choanoderm, containing brightly stained choanocyte chambers and the empty gemmule capsule in the middle. Image is intensity shaded, revealing actin organization in contractile tissues in the area outside the choanoderm. (b) Whole‐mount F‐actin staining in a N. vectensis polyp, a cnidarian model with muscles. Vertical bundles of high intensity staining through the body and in the tentacles correspond to the large retractor muscle and longitudinal tentacle muscles. (c) High resolution confocal image of the pinacoderm of the E. muelleri showing irregular organization of F‐actin bundles (highlighted in magenta). These bundles are aligned between neighboring cells, and dense actin plaques represent points of cell–cell contact. (d) High resolution confocal image of a retractor muscle in N. vectensis. The large vertical actin bundles belong to the retractor muscle, while the thin bundles running perpendicular constitute the circular body musculature. Scale bars (a, b) 200 μm and (c, d) 30 μm
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Myosin II heavy chain isoforms and transcription factors associated with different contractile tissues. The pre‐animal duplication of myosin II heavy chain (MyHC) has resulted in a separation of function of the two isoforms (stMyHC and nmMyHC) in all studied animals. The highlighted areas show highly generalized cellular context in which these have been shown to function. Red highlighting represents a muscle context and green highlighting represents a non‐muscle context. On the right, filled boxes signify that the transcription has been shown to play an important role in cell fate determination, or in the specified contractile context. If sponge contractile tissues are homologous to bilaterian muscle, the clearest expectation would be that they contain stMyHC and their differentiation is dependent on MRTF/Mef‐2 interactions
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Sponge migratory cells and body plan plasticity. (a) In the freshwater sponge model, Ephydatia muelleri, time‐lapse video illustrates cell motility over a 500‐s time span. Location of tracked cells at time 0 s (left panel) and time 500 s (middle panel). Right panel shows tracers of tracked cells, circles mark position at T = 0 s and arrowheads mark position at T = 500 s. (b) Time series illustrating the rearrangement of excurrent canal system (traced in red) over a 23‐hr time frame. g, gemmule
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