Choanoflagellates, choanocytes and animal multicellularity

Abstract

It is widely accepted that multicellular animals (metazoans) constitute a monophyletic unit, deriving From ancestral choanoflagellate-like protists that gave rise to simple choanocyte-bearing metazoans. However, a re-assessment of molecular and histological evidence on choanoflagellates, sponge choanocytes, and other metazoan cells reveals that the status of choanocytes as a fundamental cell type in metazoan evolution is unrealistic. Rather, choanocytes are specialized cells that develop from non-collared ciliated cells during sponge cmbryogenesis. Although choanocytes of adult sponges have no obvious homologue among metazoans, larval cells transd rentiating into choanocytes at metamorphosis do have such homologues. The evidence reviewed here also indicates that sponge larvae are architecturally closer than adult sponges to the remaining metazoans. This may mean that the basic multiccllular organismal architecture from which diploblasts evolved, that is, the putative planktonic archimetazoan, was more similar to a modern poriferan larva lacking choanocytes than to an adult sponge. Alternatively, it may mean that other metazoans evolved from a neotcnous larva of ancient sponges. Indeed, the Porifera possess some features of intriguing evolutionary significancc: ( I ) widespread occurrence of internal lertilization and a notable diversity of' gastrulation modes, (2) dispersal through architecturally complcx lecithotrophic larvae, in which an ephemeral archenteron (in dispherula larvae) and multiciliated and syncytial cells (in trichimella larvae) occur, (3) acquisition of direct development by some groups, and (4) replacerncnt of choanocyte-based lilter-feeding by carnivory in some sponges. Together, thcse features strongly suggest that the Porifera may have a longer and more complicated evolutionary history than traditionally assumed, and also that the simple anatomy of modern adult spongcs may have resulted from a secondary simplification. This makes the idea of a neotenous evolution less likely than that of a larva-like choanocyte-lacking archimetazoan. From this perspective, the view that choanoflagellates may be simplified sponge-derived metazoans, rather than protists, emerges as a viable alternative hypothesis. This idea neither conflicts with the available evidence nor can be disproved by it, and must be specifically re-examined by further approaches combining morphological and molecular information. Interestingly, several microbial lincages lacking choanocyte-like morphology, such as Corallochytrea, Cristidiscoidea, Ministeriida, and Mesomycetozoea, have recently been placed at the boundary between fungi and animals, becoming a promising source of information in addition to the choanoflagellates in the search for the unicellular origin of animal multicellularity.