The significance of sponges for comparative studies of developmental evolution

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

A muscle-related contractile tissue specified by myocardin-related transcription factor activity in Porifera

“…Together with observations that endopinacoderm-lined water canals can remodel in response to water flow dynamics (49,50), these data support a model in which MRTF-mediated environmental feedback mechanisms drive the development of the endopinacoderm. We speculate that this could be the rule rather than the exception in sponges, and it is conceptually plausible that this reflects the ancestral condition.…”

“…Finally, the role of MRTF in endopinacoderm differentiation helps to explain the plasticity and regenerative capacity of sponge tissues. Evidently without the need for the intrinsic positional cues characteristic of embryogenesis, sponges can develop normally from archeocyte-enriched aggregates and from gemmules, and adult tissues can remodel in response to flow dynamics 43,44 , 45,46 . In vertebrates, MRTF is an actin-regulated force-sensor involved in muscle plasticity and regeneration 21,47,48 , and our data indicate that similar mechanisms are operating in E. muelleri.…”

The Single-Celled Ancestors of Animals: A History of Hypotheses

“…Unlike hypothesized homologies between ciliates and animals, the inferred homology of the collar complex in animals and choanoflagellates survived molecular and biochemical analyses, which confirmed that the collar is composed of homologous cytoskeletal filaments in both choanoflagellates, sponges, and other animals (reviewed in (Brunet and King 2017;Leadbeater 2015)). The hypothesis of the homology of the collar complex -proposed on morphological grounds in the 19 th century -thus appears to have been predictive (Colgren and Nichols 2020) and is now accepted by most authors (but see (Mah, Christensen-Dalsgaard, and Leys 2014;Sogabe et al 2019) for exceptions and (Brunet and King 2017; Colgren and Nichols 2020; Myers 2019) for responses).…”

Distributed physiology and the molecular basis of social life in eusocial insects

“…Though the soma-germline distinction is blurry in some eusocial lineages (e.g. in the ant taxa of Harpegnathus and Ooceraea where workers retain some reproductive potential) the same can be said of many multicellular organisms (plants, worms, sponges) [19][20][21] .…”