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 approvedandthe 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 interests: of Nonedeclared.
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 contributed All to conception design,and manuscrip All authors All 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 CompetingNone interests: 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
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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 and approved 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 interests: of Nonedeclared. 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 Development of neuro-muscular and arms) in the anterior and the development in cephalopods. complex visceropallium (mantle, funnel and Hox genes are described as general In our lab, we focus on the neuro- visceres) in the posterior (stages 22 to antero-posterior organizers in muscular complex. Developmental hatching at stage 30) (Figure 2B). Bilateria, showing a colinear pattern studies have identified a molluscan Importantly, at the same time, the of expression, with anterior-class basic design (bauplan) in the future adult dorsal and ventral parts genes expressed in more rostral cephalopod nervous system, including a differentiate (e.g. all skin components domains than posterior-class ones classical set of paired ganglia: cerebral, allowing camouflage8). Thus, these (aka the well-known “hox pedal and visceral-pleural ganglia
changes cannot be interpreted as a colinearity”). But cephalopods should (Figure 1). The nervous system
All authors All contributed to conception and design, manuscrip authors All abide by the Association Medical for Ethics (AME) ethical of rules disclosure. simple flexion of the preexisting be added to the list of « bizarre » emerges as distant ganglia, some of CompetingNone interests: declared. embryonic axis. Contrary to other species with no clear correspondence them merging and fusing later to form
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the cephalopod CNS (Figure 2C). This development of the brain is similar between cephalopod species although the timing of lobe formation and rearrangement seems to be related to the mode of life at hatchling13. In Sepia officinalis, at the beginning of organogenesis (stages 15 to 20), the cerebroid ganglia emerge on both sides of the future mouth, the visceral ganglia develop on both sides of the mantle and the pedal ganglia emerge between arms 4 and 514. All these ganglia begin condensing and merging to each other from stage 23 to form the brain in the embryo’s head (Figure
2C). As for the PNS, both stellate ganglia begin to develop on the left and right sides of the mantle at the edges of the presumptive shell sac from stage 19 and intrabrachial ganglia take place all along the arms’ crown and develop into the arms from stage 17. At the same time the Figure 2: Development of Sepia officinalis and orientation. A: General organisation of muscular system develops: the mantle the embryo from stage 14 to stage 30 at hatching. Stages are indicated below. B: growth as a disk in the centre of the Development of the muscular structures involved in locomotory functions. The first and second drawings are in aboral view, the third in ventral view, the fourth in dorsal embryo; the shell sac invaginates and view. C: Development of the nervous system from sparse ganglia to the brain. The two is closed at stage 20, the two paired last drawings are in ventral view. L: left R: right. m: mantle; fp: funnel pouch; ft: funnel elements of the funnel are disposed in tube; e: eye; a1 to a5: arm 1 to arm 5; ss: shell sac; Color code of ganglia: see figure 1. lateral parts of the mantle for the
pouches and posteriorly for the tube officinalis embryos, otx expression is very late during the development16
(Figure 2B); the arms appear as buds observed in cerebral and pedal suggesting that the regionalization in the periphery of the embryo, they ganglia, which will constitute anterior could be accurate only for the SBM; the grow and the differences between parts of the adult central nervous SPM in the dorsal position could then
arms and tentacles are already visible system (all the SPM and aSM/mSM be considered as anterior. This point
preparation,read and approved the final manuscript.
at stage 20. (anterior and medial) parts of the SBM needs further comparative studies to be t Thus, the development of the nervous (Figure 1)16. solved. system is a very complex and highly otx seems to have conserved its role Among the different genes of the coordinated process. How do ganglia for anterior CNS determination, hedgehog pathway identified in develop, how do they migrate and although the territories implicated are vertebrates, shh is the most studied and merge as lobes and how do brain sparse ganglia, and not a unique has a key role in organogenesis and in lobes mature are essential questions. central nervous tissue as in dorso-ventral organisation of the Different genes, transcription factors vertebrates or insects. In this context, vertebrate brain by acting upstream on
and morphogens have been studies in Euprymna have suggested several genes (transcription factors) Conflict interests: of Nonedeclared. characterized in lophotrochozoans that Hox genes do not play their such as Pax6 and Pax 3/717,18 (Figure (including molluscs) as playing a classical role: Lab, Hox3, and Scr, 3A). major role in the developing nervous considered as anterior genes, are In ecdysozoans Drosophila hedgehog system. We explored these genes in expressed in visceral ganglia, is necessary for proliferation initiation Sepia officinalis. corresponding to the future posterior of larval neuroblasts and in some part of the SBM (pSM), whereas the lophotrochozoan trochophore larvae, Genes and the neuromuscular most posterior Hox genes, Ant, Lox4, hh is expressed in neural cells of the complex Post 2 are expressed in pedal ganglia ventral cord/chain or in the midline Otx/orthodenticle is a transcription corresponding to aSM/mSM10. It is not territory and sensorial cells19,20. factor known to have a highly yet clear how many genes and which In vertebrates, Shh acts upstream conserved role in the differentiation of ones are expressed in the cerebroid Pax3 and Pax7, which have a role in
anterior neural structures in ganglia in Euprymna. This questions neural crests specification and in
All authors All contributed to conception and design, manuscrip authors All abide by the Association Medical for Ethics (AME) ethical of rules disclosure. metazoans from vertebrates to the regionalization of the NS versus muscular progenitors determination in CompetingNone interests: declared. brachiopods and annelids15. In Sepia the body. Otx2 is expressed in the SPM somites. In S. officinalis, Pax3/7 is
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expressed only in the pedal ganglia (thus linked to the arms) and later in the aSM but not in a dorsal position of the nervous system, and hh is not expressed within the neural ganglia areas (Figure 3B)21. Pax6 is expressed in cerebroid, optic and pedal ganglia, all of them leading to SPM and aSM/mSM. 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 area21 (Figure 3B). 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 Figure 3: Neuromuscular development in vertebrate (A) and in Sepia officinalis (B). patterns of apterous do not suggest A below: molecular pathways of genes involved in the dorso-ventral setting up of any role in the early dorso-ventral the CNS where the expression of Pax genes depends of the morphogen shh patterning as it is observed in other produced with a dorso-ventral gradient (inspired from the neural tube position). A groups22. Cephalopods are likely to above: factors involved in the muscular differentiation and controlled upstream by Pax genes. B below: aboral view of Sepia embryo at stage 21. hedgehog is not use unconventional pathways to expressed in the CNS and Pax6 is expressed in ganglia whatever their dorso-ventral regionalize their nervous system position. B above: all muscular territories, mantle, arms and funnel express NK4 and along the dorso/ventral axis.
Pax258, not Pax37. D: dorsal side, V: ventral side. In most developmental models, locomotor muscles setting up is under cephalopods. Moreover unlike With cephalopods being the only non- the control of myogenic regulating vertebrates or drosophila, Pax3/7 is vertebrates to produce an important
factors (MRFs), downstream Pax3 and not expressed in muscular quantity of dopamine and serotonine, preparation,read and approved the final manuscript.
23
Pax7 at least in vertebrates . MRFs progenitors; it appears more involved the knowledge of the molecular control t proteins have been putatively in ectoderme differentiation than in of the development of the dopaminergic localized in S. officinalis in muscular muscular differentiation (or at least system could help to understand its cells of arms and tentacles24 but this mesodermic area)27. evolution and the putative role of observation has not been confirmed at Because it was not possible to hedgehog. the molecular level, questioning their characterize myogenic factors in all Actually, the orientation of the role (unpublished results). An hh-like the ESTs database available in nervous system and the setting up of expression has been reported in a cephalopods and because of the associated muscular structures do not
specific sub-population of myoblasts involvement of other genes than seem determined by the same gene Conflict interests: of Nonedeclared. in S. officinalis juveniles25, but no hh expected, we suggest that network: Pax 3/7 and hh roles remain expression has been evidenced in unconventional pathways have been to be clarified in the embryo mesodermal structures leading to selected for the development of development; Otx, Pax6, possibly with muscles in the embryo and during all muscular derived structures. These apterous, and several Hox genes the main organogenesis processes25. pathways are likely linked to the intervene in the nervous system A contrario, a major expression of nervous system evolution. development (setting up, maturation, NK4 in locomotory muscle territories differentiation), and NK4 has a role in (arm, funnel, mantle) has been Conclusion locomotory muscle development. evidenced26. This gene is known to Shh is a key gene in vertebrates in the The subsequent recruitments of have an essential role in the cardiac setting up of dopaminergic and highly conserved (in protostomes and muscle setting up in other metazoans. serotoninergic systems, very deuterostomes) transcription factors
These results suggest a secondary important for the movements, the have extended their contributions in
All authors All contributed to conception and design, manuscrip authors All abide by the Association Medical for Ethics (AME) ethical of rules disclosure. recruitment of NK4 for the locomotion and the cognitive abilities. the appearance of morphological CompetingNone interests: declared. morphological innovations in novelties. These results highlight the
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