On the role of the proventricle region in reproduction and regeneration in Typosyllis antoni (Annelida: Syllidae)

Background: Syllids are a species rich annelid family possessing remarkable regenerative ability, which is not only the response after traumatic injury, but also a key step during the life cycle of several syllid taxa. In these animals the posterior part of the body becomes an epitoke and is later detached as a distinct unit named stolon. Such a sexual reproductive mode is named schizogamy or stolonization. The prostomium and the proventricle, a modified foregut structure, have been proposed to have a control function during this process, though the concrete mechanisms behind it have never been elucidated. Results: By using different experimental set-ups, histology and immunohistochemistry combined with subsequent cLSM analyzes, we investigate and document the regeneration and stolonization in specimens of Typosyllis antoni that were amputated at different levels throughout the antero-posterior body axis. The removal of the anterior end including the proventricle implies an incomplete anterior regeneration as well as severe deviations from the usual reproductive pattern, i.e. accelerated stolonization, masculinization and the occurrence of aberrant stolons. The detailed anatomy of aberrant stolons is described. A histological study of the proventricle revealed no signs of glandular or secretory structures. The ventricle and the caeca are composed of glandular tissue but they are not involved in the reproductive and regenerative processes. Conclusions: As in other investigated syllids, the proventricle region has a significant role during stolonization and reproduction processes in Typosyllis antoni. When the proventricle region is absent, anterior and posterior regeneration are considerably deviated from the general patterns. However, proventricle ultrastructure does not show any glandular component, thereby questioning a direct involvement of this organ itself in the control of reproduction and regeneration. Our findings offer a comprehensive starting point for further studies of regeneration and reproductive control in syllids as well as annelids in general

Morphological investigations of posttraumatic regeneration in Timarete cf. punctata (Annelida: Cirratulidae)

Introduction: Annelids exhibit great regenerative abilities, which are mainly used after injury or during reproduction. These lophotrochozoans thus represent excellent models for regeneration research. However, detailed morphological studies concerning annelid musculature and nervous system redevelopment are limited to few taxa, and do not allow for broader comparisons and general conclusions regarding common patterns amongst annelids. Results: Using immunohistochemical staining combined with confocal laser scanning microscopy (cLSM), we investigated the redevelopment of body wall musculature and nervous system during anterior and posterior posttraumatic regeneration in Timarete cf. punctata. Both regeneration processes start with wound healing, blastema formation, and blastema patterning. In posterior regeneration, this leads to the development of a new pygidium and a segment addition zone (SAZ) anterior to this structure. New segments are subsequently added in a sequential fashion. Anterior regeneration in contrast shows the formation of a new prostomium and peristomium first, followed by the simultaneous redevelopment of three segments, and an additional three segments in sequential order. Anterior muscular regeneration shows an outgrowth of longitudinal musculature from the residual body wall musculature, while circular musculature develops independently within the blastema. During posterior regeneration, new musculature becomes visible when the new segments reached a certain age. Neuronal regeneration begins with neurite outgrowth from the old ventral nerve cord in both cases, which are later forming loop structures. In anterior regeneration, the brain redevelops at the anteriormost position of the loops. Conclusions: Posterior regeneration recapitulates normal growth from a certain timepoint with serial segment development by a posterior segment addition zone. Anterior regeneration is more complex, showing similarities to larval development in matters of the order, in which prostomium, peristomium, and segments are generated. Furthermore, we demonstrate the usefulness of regeneration studies to investigate morphological structures and evolutionary processes

On the role of the proventricle region in reproduction and regeneration in Typosyllis antoni (Annelida: Syllidae)

Background: Syllids are a species rich annelid family possessing remarkable regenerative ability, which is not only the response after traumatic injury, but also a key step during the life cycle of several syllid taxa. In these animals the posterior part of the body becomes an epitoke and is later detached as a distinct unit named stolon. Such a sexual reproductive mode is named schizogamy or stolonization. The prostomium and the proventricle, a modified foregut structure, have been proposed to have a control function during this process, though the concrete mechanisms behind it have never been elucidated. Results: By using different experimental set-ups, histology and immunohistochemistry combined with subsequent cLSM analyzes, we investigate and document the regeneration and stolonization in specimens of Typosyllis antoni that were amputated at different levels throughout the antero-posterior body axis. The removal of the anterior end including the proventricle implies an incomplete anterior regeneration as well as severe deviations from the usual reproductive pattern, i.e. accelerated stolonization, masculinization and the occurrence of aberrant stolons. The detailed anatomy of aberrant stolons is described. A histological study of the proventricle revealed no signs of glandular or secretory structures. The ventricle and the caeca are composed of glandular tissue but they are not involved in the reproductive and regenerative processes. Conclusions: As in other investigated syllids, the proventricle region has a significant role during stolonization and reproduction processes in Typosyllis antoni. When the proventricle region is absent, anterior and posterior regeneration are considerably deviated from the general patterns. However, proventricle ultrastructure does not show any glandular component, thereby questioning a direct involvement of this organ itself in the control of reproduction and regeneration. Our findings offer a comprehensive starting point for further studies of regeneration and reproductive control in syllids as well as annelids in general

Nervous system regeneration in Typosyllis antoni (Annelida: Syllidae)

Annelids represent a metazoan taxon with remarkable regenerative abilities, used during reproduction as well as after injury. Although many studies of different aspects of annelid regeneration are available, detailed morphological investigations regarding the regeneration of specific organ systems such as the nervous system are scarce. Using immunohistochemical staining techniques combined with subsequent confocal laser scanning microscopy (cLSM) and a 3D-reconstruction based on histological sections of the anterior nervous system in adults for comparison, we investigated the redevelopment of the anterior and posterior nervous system during posttraumatic regeneration in Typosyllis antoni. In both processes, the first signs of a regenerated nervous system are neurites infiltrating the regeneration blastema. During posterior regeneration, the neurites are reorganized in a terminal commissure within the new pygidium. Afterwards, neuronal structures of the ventral nerve cord such as segmental nerves were developed. This occurs in conformity with the development of new segments by the reestablished posterior segment addition zone, comparable to normal growth. During anterior nervous system regeneration, the neurites form loops close to the stump of the remaining nerve cord, that attach its contralateral connectives. Later, these loops become the dorsal and ventral roots of the circumesophageal connectives and the brain reoccurs in an anteriormost position. This kind of anterior regeneration agrees with the general pattern known in annelids.MW thanks the University of Leipzig for funding by scholarship (U00048). CB was supported by a “Ramón y Cajal” fellowship by the MINECO, project n° RYC-2014-15615. MTA was supported by the Spanish Government (Programa José Castillejo) for a research stay at the University of Leipzig. This study is a contribution of the project “Macroevolutionary transitions in Syllidae” CGL2015-63593-P supported by MINECO/FEDER, UEfunds.Peer Reviewe