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Moreover, the expression of hh is exclusive of Pax6 expression: hh could have a role in the limitation of Pax6 nervous expression in Sepia officinalis as it is expressed in the border of Pax6 expression areas. Unlike vertebrates, Pax6 is expressed all along the development and the expression is not restricted to a dorsal area [ 21 ] Figure 3 B. It has been suggested in Euprymna scolopes, that apterous, a LIM-homeodomain transcription factor could share a role with Pax6 in the patterning of CNS, but expression patterns of apterous do not suggest any role in the early dorso-ventral patterning as it is observed in other groups [ 22 ].

In most developmental models, locomotor muscles setting up is under the control of myogenic regulating factors MRFs , downstream Pax3 and Pax7 at least in vertebrates [ 23 ]. MRFs proteins have been putatively localized in S.

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An hh-like expression has been reported in a specific sub-population of myoblasts in S. A contrario, a major expression of NK4 in locomotory muscle territories arm, funnel, mantle has been evidenced [ 26 ]. This gene is known to have an essential role in the cardiac muscle setting up in other metazoans. These results suggest a secondary recruitment of NK4 for the morphological innovations in cephalopods.

Cephalopoda. Embryology

Because it was not possible to characterize myogenic factors in all the ESTs database available in cephalopods and because of the involvement of other genes than expected, we suggest that unconventional pathways have been selected for the development of muscular derived structures. These pathways are likely linked to the nervous system evolution. Figure 3 : Neuromuscular development in vertebrate A and in Sepia officinalis B. A below: molecular pathways of genes involved in the dorso-ventral setting up of the CNS where the expression of Pax genes depends of the morphogen shh produced with a dorso-ventral gradient inspired from the neural tube position.

A above: factors involved in the muscular differentiation and controlled upstream by Pax genes. B below: aboral view of Sepia embryo at stage B above: all muscular territories, mantle, arms and funnel express NK4 and Pax, not Pax D: dorsal side, V: ventral side. Shh is a key gene in vertebrates in the setting up of dopaminergic and serotoninergic systems, very important for the movements, the locomotion and the cognitive abilities.

With cephalopods being the only non-vertebrates to produce an important quantity of dopamine and serotonine, the knowledge of the molecular control of the development of the dopaminergic system could help to understand its evolution and the putative role of hedgehog. The subsequent recruitments of highly conserved in protostomes and deuterostomes transcription factors have extended their contributions in the appearance of morphological novelties. These results highlight the diversity of molecular pathways recruited during evolution and the necessary carefulness regarding generalization of results obtained from a very small set of model organisms.

The authors wish to thank past and present members of the team who contributed with data and discussions to the ideas presented here.

The Evolution and Development of Cephalopod Chambers and Their Shape

Young J Z. Brain, behaviour and evolution of cephalopods. Symposia of the zoological society of London: Academic press; ; Kier WM. Muscle development in squid: ultrastructural differentiation of a specialized muscle fiber type. J Morphol.

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  4. Budelmann BU. The cephalopod nervous system: what evolution has made of the molluscan design.

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    In: Breidbach O and Kutsch W, editors. The nervous system of invertebrates: an evolutionary and comparative approach: Birkhauser Verlag, Basel; Nixon M, Young JZ. The brain and lives of cephalopods. Oxford University press; Naef A. Die Cephalopoden. Embryologie, Fauna Flora Golf Neapel.

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    Smithsonian Institution Press, Washington, ;p. Sepia officinalis: a new biological model for eco-evo-devo studies. J Exp Mar Biol Ecol. Lemaire J. Bull Soc Zool France. Cephalopod Behaviour. Cambridge, U. Boletzky Sv. Cephalopod development and evolutionary concepts. Paleontology and neontology of cephalopods. San Diego: Academic Press. Cephalopod Hox genes and the origin of morphological novelties. Med Sci Paris. Lemons D, McGinnis W. Genomic evolution of Hox gene clusters. Nixon M, Mangold K. J Mar Sci Tech. Lichtneckert R, Reichert H. Anteroposterior regionalization of the brain: genetic and comparative aspects.

    Adv Exp Med Biol. Gene Expr Patterns.


    Sonic Hedgehog signaling in the mammalian brain. J Neurochem. Cereb Cortex. The transcription factor, Pax6, is required for cell proliferation and differentiation in the developing cerebral cortex.

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    Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp. I and H. Dev Biol. Shh and Pax6 have unconventional expression patterns in embryonic morphogenesis in Sepia officinalis Cephalopoda. Evol Dev. Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. Muscle differentiation in tentacles of Sepia officinalis Mollusca is regulated by muscle regulatory factors MRF related proteins.

    Dev Growth Differ. A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis mollusca mantle. Dev Dyn.

    How the Squid Lost Its Shell

    Somatic muscle development in Sepia officinalis cephalopoda - mollusca : a new role for NK4. Emergence of sensory structures in the developing epidermis in sepia officinalis and other coleoid cephalopods. J Comp Neurol. Cephalopod development: what we can learn from differences.