The endoskeleton is a distinctive feature of echinoderms and consists of a true skeletal tissue with a complex microstructure (stereome). Skeletal elements can be present also in larval stages, although they differ markedly among classes. Therefore, the comparative study of larval skeletogenesis in different echinoderm classes can provide insights into the origin and evolution of this character. In this study we analysed the skeletogenic process in the crinoid Antedon mediterranea, which represents the basal echinoderm class, and the ophiuroid Amphiura filiformis. In A. mediterranea the doliolaria and the post-metamorphic pentacrinoid stages were mainly investigated, whereas in A. filiformis the blastula, gastrula, prism and pluteus stages were analysed. Detailed morphological investigations included both light and electron (SEM, TEM) microscopy techniques. Furthermore, a preliminary molecular analysis was carried out in A. mediterranea by cloning for the first time twelve skeletogenic genes already studied in A. filiformis, and studying their expression and presence by whole mount in situ hybridization (WMISH) and Quantitative-PCR (Q-PCR). Our results confirm that in A. mediterranea, primordial pentacrinoid skeletal elements are already present in the doliolaria stage. Spicule and plate formation starts in a planar multi-branched arrangement and continues throughout the metamorphosis process, until their complete three-dimensional stereome-like architecture in the pentacrinoid stage. Sclerocytes differentiate, produce short cellular expansions and develop calcitic elements in a highly cellularized and collagen rich mesenchyme. It is still unclear, however, if these elements originate within a syncytium. Differently, in A. filiformis thin tri-radiate and three-dimensional spicules are formed by primary mesenchyme cells (PMCs), following a process very similar to that described in sea urchins. PMCs differentiate in an extremely loose mesenchyme, produce long and branched fillopodia and eventually form a syncytium where calcium carbonate is deposited without furtherly developing in a stereom microstructure. Preliminary molecular analysis indicates that skeletogenesis gene orthologues of A. filiformis are present and expressed in areas of active skeleton formation also in the crinoid, suggesting that the overall genetic program for skeleton development was already present in the ancestor groups of echinoderms and has been conserved in all the five extant classes for several millions of years. Interestingly, in terms of skeletogenesis processes, the data obtained so far in different classes, comparing larval stages characterized by different life-style and cycle, indicate indeed that the cellular mechanisms can significantly diverge among groups adapting to specific functional requirements. In this view the skeleton of the lecitotrophic doliolaria, which represents the primordium of a persisting adult stereome structure, could be the primitive adaptive solution for these short-range dispersion larvae; in contrast, the specialized temporary skeleton of planktotrophic ophiuroid larvae could be an advanced strategy designed to maximize long-range dispersion capabilities. Further comparative studies on skeleton formation in different echinoderm classes, and particularly in crinoids, are necessary to complete the knowledge about its evolution.

Larval skeletogenesis in the crinoid antedon Mediterranea and the ophiuroid amphiura filiformis: a morphological, molecular and evolutionary approach / B. Cambiaghi, C. Ferrario, S. Mercurio, F. Bonasoro, M. DANIELA CANDIA CARNEVALI, P. Oliveri, M. Sugni. ((Intervento presentato al 80. convegno Convegno dell'Unione Zoologica Italiana-UZI tenutosi a Roma nel 2019.

Larval skeletogenesis in the crinoid antedon Mediterranea and the ophiuroid amphiura filiformis: a morphological, molecular and evolutionary approach

C. Ferrario;S. Mercurio;F. Bonasoro;M. Sugni
2019

Abstract

The endoskeleton is a distinctive feature of echinoderms and consists of a true skeletal tissue with a complex microstructure (stereome). Skeletal elements can be present also in larval stages, although they differ markedly among classes. Therefore, the comparative study of larval skeletogenesis in different echinoderm classes can provide insights into the origin and evolution of this character. In this study we analysed the skeletogenic process in the crinoid Antedon mediterranea, which represents the basal echinoderm class, and the ophiuroid Amphiura filiformis. In A. mediterranea the doliolaria and the post-metamorphic pentacrinoid stages were mainly investigated, whereas in A. filiformis the blastula, gastrula, prism and pluteus stages were analysed. Detailed morphological investigations included both light and electron (SEM, TEM) microscopy techniques. Furthermore, a preliminary molecular analysis was carried out in A. mediterranea by cloning for the first time twelve skeletogenic genes already studied in A. filiformis, and studying their expression and presence by whole mount in situ hybridization (WMISH) and Quantitative-PCR (Q-PCR). Our results confirm that in A. mediterranea, primordial pentacrinoid skeletal elements are already present in the doliolaria stage. Spicule and plate formation starts in a planar multi-branched arrangement and continues throughout the metamorphosis process, until their complete three-dimensional stereome-like architecture in the pentacrinoid stage. Sclerocytes differentiate, produce short cellular expansions and develop calcitic elements in a highly cellularized and collagen rich mesenchyme. It is still unclear, however, if these elements originate within a syncytium. Differently, in A. filiformis thin tri-radiate and three-dimensional spicules are formed by primary mesenchyme cells (PMCs), following a process very similar to that described in sea urchins. PMCs differentiate in an extremely loose mesenchyme, produce long and branched fillopodia and eventually form a syncytium where calcium carbonate is deposited without furtherly developing in a stereom microstructure. Preliminary molecular analysis indicates that skeletogenesis gene orthologues of A. filiformis are present and expressed in areas of active skeleton formation also in the crinoid, suggesting that the overall genetic program for skeleton development was already present in the ancestor groups of echinoderms and has been conserved in all the five extant classes for several millions of years. Interestingly, in terms of skeletogenesis processes, the data obtained so far in different classes, comparing larval stages characterized by different life-style and cycle, indicate indeed that the cellular mechanisms can significantly diverge among groups adapting to specific functional requirements. In this view the skeleton of the lecitotrophic doliolaria, which represents the primordium of a persisting adult stereome structure, could be the primitive adaptive solution for these short-range dispersion larvae; in contrast, the specialized temporary skeleton of planktotrophic ophiuroid larvae could be an advanced strategy designed to maximize long-range dispersion capabilities. Further comparative studies on skeleton formation in different echinoderm classes, and particularly in crinoids, are necessary to complete the knowledge about its evolution.
23-set-2019
Settore BIO/05 - Zoologia
Unione Zoologica Italiana
Larval skeletogenesis in the crinoid antedon Mediterranea and the ophiuroid amphiura filiformis: a morphological, molecular and evolutionary approach / B. Cambiaghi, C. Ferrario, S. Mercurio, F. Bonasoro, M. DANIELA CANDIA CARNEVALI, P. Oliveri, M. Sugni. ((Intervento presentato al 80. convegno Convegno dell'Unione Zoologica Italiana-UZI tenutosi a Roma nel 2019.
Conference Object
File in questo prodotto:
File Dimensione Formato  
Sugni UZI 2019.pdf

accesso aperto

Tipologia: Pre-print (manoscritto inviato all'editore)
Dimensione 337.73 kB
Formato Adobe PDF
337.73 kB Adobe PDF Visualizza/Apri
Pubblicazioni consigliate

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/2434/678536
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus ND
  • ???jsp.display-item.citation.isi??? ND
social impact