The origin of animal multicellularity and cell differentiation

Brunet, Thibaut; King, Nicole

doi:10.1101/161695

Cited by 20 publications

(31 citation statements)

References 215 publications

(42 reference statements)

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“…Superficially both types of collared cells are similar to each other (Brill, 1973;Amano and Hori, 1996;Maldonado, 2004;Gonobobleva and Maldonado, 2009), which has been explored in many reviews (see ref. : Brunet and King, 2017). But already in the first detailed description of a choanocyte kinetid we found that it is fundamentally different from that of choanoflagellates (Karpov and Efremova, 1994).…”

Section: Why We Need the Detailed Study Of Kinetids?mentioning

confidence: 91%

“…These findings further supported the hypothesis that the metazoan ancestor was similar to choanoflagellates. The phylogeny of multicellular animals with an origin from a choanoflagellate-like ancestor has been elaborated in the recent reviews (Nielsen, 2012;CavalierSmith, 2016;Brunet and King, 2017).…”

Section: Do Choanoflagellates Represent the Image Of A Metazoan Ancesmentioning

confidence: 99%

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Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Pozdnyakov¹,

Agniya

Alexander

et al. 2017

Protistology

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SummaryAny discussion of the origin of Metazoa during the last 150 years and particularly in the recent years when the sister relationship of choanoflagellates and Metazoa was unambiguously shown by molecular phylogeny refers to the similarity of sponge choanocytes to choanoflagellates. These two types of collared radially symmetric cells are superficially similar with respect to the presence of microvilli around a single flagellum and flat mitochondrial cristae which are common for many eukaryotes. But a comparison of the most informative structure having a stable phylogenetic signal, the flagellar apparatus or kinetid, has been neglected. The kinetid is well studied in choanoflagellates and is rather uniform, but in choanocytes this structure has been investigated in the last five years and is represented by several types of kinetids. Here we review the kinetid structure in choanocytes of Porifera to establish the most conservative type of kinetid in this phylum. The detailed comparison of this kinetid with the flagellar apparatus of choanoflagellates demonstrates their fundamental difference in many respects. The choanocyte kinetid contains more features which can be considered plesiomorphic for the opisthokonts than the kinetid of the choanoflagellates. Therefore, the hypothesis about the origin of Porifera, and consequently of all Metazoa directly from choanoflagellate-like unicellular organism is not confirmed by their kinetid structure.

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Section: Why We Need the Detailed Study Of Kinetids?mentioning

confidence: 91%

Section: Do Choanoflagellates Represent the Image Of A Metazoan Ancesmentioning

confidence: 99%

Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Pozdnyakov¹,

Agniya

Alexander

et al. 2017

Protistology

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“…Sponges, like the rest of metazoans, produce differentiated sperm and egg, exhibit conserved developmental gene expression patterns, have epithelia, contain a suite of metazoan-specific genes (for example, Wnt ), and develop through a clonal process of serial cell division [14–17]. Sponge collar cells, which bear a single flagellum surrounded by a collar of microvilli, resemble the cell morphology of the choanoflagellates ([18, 19] but see [20]), the closest living relatives of metazoans [21], which was interpreted as further support for the notion that sponges are the sister lineage to the rest of metazoans.…”

Section: A Brief Historical Perspectivementioning

confidence: 99%

“…For example, the conservation of the cadherin-repeat encoding gene hedgling in choanoflagellates, sponges, and cnidarians suggests that it was present in the Urmetazoan, despite its absence from the genomes of ctenophores, placozoans, and bilaterians [e.g., 59, 60]. Similarly, the collar cells found today in choanoflagellates, sponges, cnidarians and many bilaterians likely appeared in the Urmetazoan, despite their absence from ctenophores and most ecdysozoans [19]. …”

Section: Implications Of the Controversy For Reconstructing The Urmetmentioning

confidence: 99%

Embracing Uncertainty in Reconstructing Early Animal Evolution

2017

Self Cite

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The origin of metazoans, one of the major transitions in evolution, remains mysterious. While many key aspects of metazoan origins can be reconstructed by comparing living organisms within a robust phylogenetic framework, uncertainty regarding the evolutionary relationships among sponges, ctenophores and the remainder of metazoan diversity has proven to be a major barrier. Comparative morphology and some phylogenomic analyses support the view that sponges represent the sister lineage to the rest of the metazoans, while other competing phylogenomic analyses strongly support ctenophores, a phylum of carnivorous, gelatinous marine organisms, as the sister lineage. Here, we explore why different phylogenomic studies yield different answers and discuss the implications of the two alternative hypotheses for understanding the origin of metazoan multicellularity. Reconstruction of ancient evolutionary radiations, like the one that gave rise to metazoans, is devilishly difficult and will likely require broader sampling of sponge and ctenophore genomes, improved analytical strategies, and critical analyses of the phylogenetic distribution and molecular mechanisms underlying apparently conserved traits. Rather than staking out positions in favor of the ctenophore-sister or the sponge-sister hypothesis, we submit that research programs aimed at understanding the biology of the first metazoans should embrace the uncertainty surrounding early metazoan evolution in their experimental designs.

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“…The rosettes resemble early embryonic stages of holoblastic organisms (Brunet & King, 2017). Indeed, following Haeckel's (1892) blastaea hypothesis and the observations that numerous organisms include a ciliated blastula stage of the life cycle, recent investigators (Arendt, 2005;Nielsen, 2008) have proposed that the ancestors of animals were motile spheres of ciliated cells.…”

Section: The Origin Of Multicellular Life Cyclesmentioning

confidence: 97%

Evolutionary transitions revisited: Holobiont evo‐devo

Gilbert

2019

J Exp Zool Pt B

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John T. Bonner lists four essential transformations in the evolution of life: the emergence of the eukaryotic cell, meiosis, multicellularity, and the nervous system. This paper analyses the mechanisms for those transitions in light of three of Dr. Bonner's earlier hypotheses: (a) that the organism is its life cycle, (b) that evolution consists of alterations of the life cycle, and (c) that development extends beyond the body and into interactions with other organisms. Using the notion of the holobiont life cycle, this paper attempts to show that these evolutionary transitions can be accomplished through various means of symbiosis. Perceiving the organism both as an interspecies consortium and as a life cycle supports a twofold redefinition of the organism as a holobiont constructed by integrating together the life cycles of several species. These findings highlight the importance of symbiosis and the holobiont development in analyses of evolution.

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The origin of animal multicellularity and cell differentiation

Cited by 20 publications

References 215 publications

Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship

Embracing Uncertainty in Reconstructing Early Animal Evolution

Evolutionary transitions revisited: Holobiont evo‐devo

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