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Cephalopod Development: What We Can Learn from Differences Development L Bonnaud-Ponticelli1, Y Bassaglia1,2*

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Cephalopod Development: What We Can Learn from Differences Development L Bonnaud-Ponticelli1, Y Bassaglia1,2* Page 1 of 5 Review Cephalopod development: what we can learn from differences Development L Bonnaud-Ponticelli1, Y Bassaglia1,2* Abstract diversity of body plan organisation molecular control of the development Introduction (Figure 1). in an evolutionary perspective. The molluscan neuro-muscular Cephalopods are the most intriguing system shows extreme diversity. group, presenting not only an original Discussion Cephalopods present an original body body plan among molluscs, The authors have referenced some of plan, a derived neuro-muscular particularly regarding the locomotory their own studies in this review. The complex and a development with system, but also obvious convergences protocols of these studies have been drastic changes in the antero- with vertebrates, especially regarding approved by the relevant ethics posterior/dorso-ventral orientation. the nervous system. The contribution committees related to the institution in of cephalopods in neurosciences, from which they were performed. Animal How it took place during evolution is an unresolved question that can be cellular physiological mechanisms to care was in accordance with the approached by the study of behaviour in vertebrates, is doubtless institution guidelines. developmental genes. Studying the - by the famous nobel work on giant expression of conserved transcription axons of the squid but also by their Cephalopods are morphological factors (Pax and NK families, otx, apt) learning and memory abilities innovators and morphogen (hedgehog) during regarded as surprising for an By contrast with the typical molluscan 1 development is a good test of the “invertebrate” . But cephalopods can design, coleoids (octopus, squids, conservation of their functions. We also be studied for themselves to cuttlefish) show a derived and underline here unexpected expression address evolutionary questions: how specialized neuro-muscular complex. patterns during cephalopod it is possible to evolve from an The brachial crown and the funnel, both development, and we aim to suggest ancestral mollusc through an presumptively derived from the that these patterns may be, at least ancestral cephalopod and which molluscan foot, and the highly muscular partly, in relation to morphological mechanisms have led to these mantle are used in the characteristic jet novelties in this clade. innovations is a crucial point in the propulsion locomotion of cephalopods. Conclusion understanding of cephalopod lineage Histological studies have shown that The expression patterns observed characteristics and also of these locomotor muscles are oblique point out the diversity of molecular neuromuscular complex evolution. striated muscles, a muscle type also pathways recruited during evolution In this context, an evo-devo identified in nematodes, annelids or 2 preparation, read approvedand the final manuscript. approach seems pertinent. These other molluscs . The nervous system of and the necessary carefulness t regarding generalization of results studies aim to characterize genes cephalopods is very different from that obtained from a very small set of controlling development, which are of other lophotrochozoans3. They have model organisms. Studying different involved in modifications of body axes no ventral nerve cord and their nervous species, with a large diversity of and patterning or morphological system is highly specialized. It includes morphology, could help to have a novelties. By comparative analyses, a peripheral nervous system (PNS) with better understanding of the variety of these studies allow inferences about stellate ganglia, nervous cords of the the genes roles and/or of the plasticity the evolutionary process but they also arms/tentacles and several sparse reveal the evolutionary plasticity of of networks. ganglia (Figure 1) and, above all, a very Conflict of interests: None declared. developmental genes and gene complex central nervous system (CNS) Introduction networks. with a brain enclosed in a cartilaginous Based on the peculiar case of Molluscs represent a very surprising capsule and associated to voluminous cephalopods, and the knowledge on metazoan clade. Including optic lobes. Described in detail in the most conserved and known Polyplacophora, Bivalvia, Gastropoda, numerous coleoid cephalopods, the transcription factors and morphogens, and Cephalopoda, they show clear brain comprises of supra- and sub- this review aims to point out the synapomorphies (shell, mantle, oesophageal masses (SPM and SBM, diversity of molecular pathways muscular foot) but present a high Figure 1) disposed between the eyes recruited during evolution and the around the oesophagus and divided necessary carefulness regarding into 25 major lobes, with specific *Corresponding author generalization of results obtained different functions4. Email: [email protected] from a too small set of model The movements and behaviour are 1 organisms. Several aspects must be All authors contributedAll to conception design,and manuscrip All authors abide by the Association Medical for Ethics (AME) ethical of rules disclosure. MNHN BOREA (UMR MNHN CNRS 7208-IRD under the control of the brain receiving Competing interests: None declared. 207-UPMC-UCBN), Paris, France considered in the study of the 2 and analysing visual input from the Université Paris Est-Créteil Val de Marne camerular eyes, which are convergent (UPEC), Créteil, France Licensee OAPL (UK) 2014. Creative Commons Attribution License (CC-BY) FOR CITATION PURPOSES: Bonnaud-Ponticelli L, Bassaglia Y. Cephalopod development: what we can learn from differences. OA Biology 2014 Apr 18;2(1):6. Page 2 of 5 Review structures with vertebrates. The giant fibre system allows very fast answers (e.g. fast jet propulsion) to environmental cues. It is generally assumed that these muscular and nervous systems have been selected concomitantly to the loss of the molluscan external protective shell during evolution. But the arguments sustaining this assumption are quite elusive justifying attempts to develop new approaches such as evo-devo studies. Development of cephalopods: an axis imbroglio Unlike other molluscs, cephalopods Figure 1: Cephalopod organisation versus mollusc organisation. Foot and shell as well have a direct development without as the anterior triangle of ganglia (cerebral, pedal, visceral) are synapomorphies of neither visible larval stage nor molluscs and are present in the ancestor.The foot is conserved in Bivalvia and metamorphosis event. Nevertheless, Gastropoda but is modified in Cephalopoda in peribuccal appendages (8 arms and 2 drastic changes in embryonic tentacles in Sepia) and funnel. The shell is regressed in Cephalopoda and the nervous orientation occur during development system is modified. Brachial ganglia are novelties in relation to the arm appearance, within the protecting egg capsule. stellate ganglia are unique and most of the ganglia are divided in several lobes and The development of cephalopods is concentrated into a brain, composed of a supraoesophageal mass, SPM with issued well described since the early 20th from cerebral ganglia, and a sub-oesophageal mass, SBM issued from pedal and visceral ganglia. The optic lobes, connected to the eyes, represent 90% of the CNS. A : anterior ; century and the masterwork of Naef5. P : posterior ; a: arm; e : eye ; g : gill ; Gg: ganglion; dt : digestive tube ; t: tentacle. All cephalopods have telolecithal Puncted line : nerve and/or connectives. eggs and present a discoidal cleavage unlike other molluscs in which a total classical developmental models, between regionalization and hox genes and spiral segmentation occurs. In especially vertebrates, the adult expression; in fact, cephalopod hox Sepia officinalis, the model we work antero-posterior axis is very different genes expression seems to correlate on in the lab in an eco-evo-devo from the embryonic axis underlying better with morphological novelties10. perspective, cleavage leads to a flat, bilateral symmetry and runs from the Interestingly, the hypothesis that hox disk-shaped embryo until stage 14 embryonic oral side (yolk side) to colinearity is only the result of an (based on Lemaire’s system) where aboral side, which correspond exaptation has been presented in preparation, read andapproved the final manuscript. 6,7 11 organogenesis starts (Figure 2) . respectively to the future anterior and vertebrates . As in other clades t Until stage 20, the flat embryo shows posterior part. This is reflected in the (echinoderms, tunicates)12, the a clear bilateral symmetry axis, vocabulary used in the field, which recruitment of hox genes in other parallel to the yolk surface, sometime describes an “embryonic orientation” functions than the specification of an described as antero-posterior due to and an “adult/physiological antero-posterior axis may provide an the position of the future mouth. orientation” 9 (Figure 2). explanation to the innovative body Progressively, the embryo takes This imbroglio points out that, even architectures found in cephalopods. volume (stages 19 to 21) and stick up based on classical orientated The question of the existence and the perpendicularly to the yolk with a structures (the mouth in an anterior nature of “master organizing genes” in Conflict of interests: None declared. flexion of all the body (Figure 2A). The and ventral position), morphology is cephalopods remains unanswered. future adult antero-posterior axis is not sufficient to understand the marked by the cephalopodium (head orientation of the body plan during
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