Origins of the other metazoan body plans: the evolution of larval forms

Raff, Rudolf A.

doi:10.1098/rstb.2007.2237

Cited by 139 publications

(115 citation statements)

References 40 publications

(40 reference statements)

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“…This study revealed that in modern echinoids, changes to mesodermal GRN architecture have occurred more frequently than alterations to ectodermal GRN architecture. These results support the notion that GRN architecture evolves at different rates (81), and provide an in-principle explanation for the rapid evolution observed in both cidaroid and euechinoid sea urchin lineages that have convergently and independently evolved directdeveloping larval forms (53). It remains to be determined in future research whether the shared regulatory states between cidaroids and euechinoids elucidated here are the product of conserved stretches of genomic DNA hardwired in the cis-regulatory regions of orthologous regulatory genes or the result of diverged cis-regulatory modules producing similar developmental outcomes.…”

Section: Evolution Of Global Embryonic Domains In Early Development Ofsupporting

confidence: 82%

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Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

Proc. Natl. Acad. Sci. U.S.A.

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Developmental gene regulatory networks (GRNs) are assemblages of gene regulatory interactions that direct ontogeny of animal body plans. Studies of GRNs operating in the early development of euechinoid sea urchins have revealed that little appreciable change has occurred since their divergence ∼90 million years ago (mya). These observations suggest that strong conservation of GRN architecture was maintained in early development of the sea urchin lineage. Testing whether this holds for all sea urchins necessitates comparative analyses of echinoid taxa that diverged deeper in geological time. Recent studies highlighted extensive divergence of skeletogenic mesoderm specification in the sister clade of euechinoids, the cidaroids, suggesting that comparative analyses of cidaroid GRN architecture may confer a greater understanding of the evolutionary dynamics of developmental GRNs. Here I report spatiotemporal patterning of 55 regulatory genes and perturbation analyses of key regulatory genes involved in euechinoid oral-aboral patterning of nonskeletogenic mesodermal and ectodermal domains in early development of the cidaroid Eucidaris tribuloides. These results indicate that developmental GRNs directing mesodermal and ectodermal specification have undergone marked alterations since the divergence of cidaroids and euechinoids. Notably, statistical and clustering analyses of echinoid temporal gene expression datasets indicate that regulation of mesodermal genes has diverged more markedly than regulation of ectodermal genes. Although research on indirectdeveloping euechinoid sea urchins suggests strong conservation of GRN circuitry during early embryogenesis, this study indicates that since the divergence of cidaroids and euechinoids, developmental GRNs have undergone significant, cell typebiased alterations.gene regulatory network | echinoderms | sea urchin embryogenesis | embryonic axis specification | echinoids

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Section: Evolution Of Global Embryonic Domains In Early Development Ofsupporting

confidence: 82%

“…Alterations to GRN architecture have occurred frequently throughout the network since their divergence. In addition, these results offer an in-principle explanation for the rapid changes in developmental processes during the convergent evolution of direct-developing, nonfeeding sea urchins (50)(51)(52)(53).…”

mentioning

confidence: 77%

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Erkenbrack

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…An emerging research direction focuses on comparative studies of neuronal circuitry in diverse marine larvae. Even though the evolutionary origin and ancient versus modern origin of larvae is still debated [73,74], our results support the view that the larval eyes and brain of annelids (and probably other spiralian) represent more closely an ancestral stage of brain evolution [8]. Comparing circuits in spiralian larval nervous systems to the circuits of cnidarian larvae and the ciliated larvae of certain marine deuterostomes (e.g.…”

Section: Discussionsupporting

confidence: 80%

Origin and early evolution of neural circuits for the control of ciliary locomotion

Jékely

2010

Proc. R. Soc. B.

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Behaviour evolved before nervous systems. Various single-celled eukaryotes (protists) and the ciliated larvae of sponges devoid of neurons can display sophisticated behaviours, including phototaxis, gravitaxis or chemotaxis. In single-celled eukaryotes, sensory inputs directly influence the motor behaviour of the cell. In swimming sponge larvae, sensory cells influence the activity of cilia on the same cell, thereby steering the multicellular larva. In these organisms, the efficiency of sensory-to-motor transformation (defined as the ratio of sensory cells to total cell number) is low. With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible. This may have first occurred in a ciliated swimming stage of the first eumetazoans. The first axons may have had en passant synaptic contacts to several ciliated cells to improve the efficiency of sensory-to-motor transformation, thereby allowing a reduction in the number of sensory cells tuned for the same input. This could have allowed the diversification of sensory modalities and of the behavioural repertoire. I propose that the first nervous systems consisted of combined sensory-motor neurons, directly translating sensory input into motor output on locomotor ciliated cells and steering muscle cells. Neuronal circuitry with low levels of integration has been retained in cnidarians and in the ciliated larvae of some marine invertebrates. This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection. The sensory-motor nervous systems of cnidarians and ciliated larvae of diverse phyla show that brains, like all biological structures, are not irreducibly complex.

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“…THE PROTOSTOME -DEUTEROSTOME TOOLKIT The similarity of a variety of complex morphogenetic pathways across protostomes and deuterostomes (based initially on studies of Drosophila, Cenorhabditis and Mus, but recently expanding to a more phylogenetically diverse array of animals) led to the conclusion that their last common ancestor not only possessed these developmental systems, but the complex morphologies that they produce in modern organisms (Slack et al 1993;De Robertis & Sasai 1996;Ohno 1996;Valentine et al 1999;Carroll et al 2001;Erwin & Davidson 2002;Erwin 2006;De Robertis 2008;Raff 2008). …”

Section: Introductionmentioning

confidence: 99%

Early origin of the bilaterian developmental toolkit

Erwin

2009

Phil. Trans. R. Soc. B

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Whole-genome sequences from the choanoflagellate Monosiga brevicollis , the placozoan Trichoplax adhaerens and the cnidarian Nematostella vectensis have confirmed results from comparative evolutionary developmental studies that much of the developmental toolkit once thought to be characteristic of bilaterians appeared much earlier in the evolution of animals. The diversity of transcription factors and signalling pathway genes in animals with a limited number of cell types and a restricted developmental repertoire is puzzling, particularly in light of claims that such highly conserved elements among bilaterians provide evidence of a morphologically complex protostome–deuterostome ancestor. Here, I explore the early origination of elements of what became the bilaterian toolkit, and suggest that placozoans and cnidarians represent a depauperate residue of a once more diverse assemblage of early animals, some of which may be represented in the Ediacaran fauna (c. 585–542 Myr ago).

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Origins of the other metazoan body plans: the evolution of larval forms

Cited by 139 publications

References 40 publications

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

Origin and early evolution of neural circuits for the control of ciliary locomotion

Early origin of the bilaterian developmental toolkit

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