A worm called Anton

In 2010 when I still had my lab in Leipzig (Germany) we started noticing that a species of syllid annelids can be frequently found in our warm water aquariums. As we were working on annelid phylogenomics, we were quite happy having easy access to these animals in Leipzig, a place that is at least several hundreds kilometers away from any access to the sea. We sequenced the transcriptome, but couldn’t identify the animal (neither by morphology nor barcoding) to the species level. The following years, the population remained stable. Ovbviously they were reproducing quite well and we usually had a peak of individuals in late spring. We realized that this so far undescribed species has the potential to be our lab rat for different research questions, e.g., on syllid reproduction and regeneration. Consequently, we decided to formally describe this animal (Aguado et al. 2014). Even though we could not indicate its native geographical range of occurrence, we described it in such detail that it should be recognized when found outside our aquariums. In honor of the newborn son (Anton Helm) of one member of our research team we named the species Typosyllis antoni (Fig. 1).

syllis_antoni

Fig. 1: Adult individual of Typosyllis antoni 

This species can be distinguished by molecules and morphology from all other so far described Syllinae (a group of syllids where this species belongs to). Since its description in 2014 T. antoni fastly became one of the best studied syllids and polychaetes in general. We carefully described the external and internal anatomy in the formal species description, where we especially focussed on the muscle system. Moreover, an adult transcriptome has been published (here still called Syllis sp.) within the framework of a phylogenomic analyses of annelids in Weigert et al. (2014). Recently, we published the complete mitochondrial genome sequence of this and some other syllid species, which show a surprisingly variable order of genes when compared to other annelids (Aguado et al. 2016). However, the most fascinating part about syllid biology is their reproduction.

repmodessyll

Fig. 2: Sexual reproductive modes in syllids are epigamy (a) and schizogamy (b)

There are two reproductive modes in Syllidae, called epigamy and schizogamy, and both modes involve strong anatomical and behavioural changes. Epigamic reproduction (Fig. 1a) involves the transformation of the adult body into an epitoke, which will swim to the surface, spawn the gametes and die. Usually this behaviour is synchronized across population (e.g., triggered by the lunar cycle) to enhance the probability of successful fertilization. Epigamy is also found in other annelids, such as nereidids or eunicids. In contrast, during schizogamy, the posterior part of the adult is transformed into a stolon (or several stolons), which carries the gametes. Again these stolons swim to the surface and release gametes, while dying. However, the parental animal remains in its natural habitat and regenerates its posterior end. Such animals can usually go through several cycles of stolonization. Interestingly, this type of reproduction seems to have evolved twice within Syllidae (Aguado et al. 2007).

A unique morphological structure found in Syllidae is the proventricle, which is considered as a synapomorphy for this group. The proventricle is a muscular structure with radially arranged striated muscle cells surrounding the gut. These cells consist of usually only one or two sarcomeres with up to 100 μm length, being the longest known sarcomeres within the Metazoa! Interestingly, it has been proposed that the proventricle
controls the process of stolonization, while also promoting the regeneration of the posterior end. However, how this control is achieved remained unclear, even though it was speculated that mediation via hormones seems plausible.To investigate this question, we started regeneration experiments in T. antoni, where we used different cutting sites (Fig. 3) across the animals to analyse what the role of the proventricle could be. Moreover, we took a detailed look at the proventricle using histology.

cutting

Fig. 3: Drawing of Typosyllis antoni illustrating the different cutting sites for our regeneration experiments

The animals usually show signs of regeneration and were also able to regenerate new heads and tails. However, there were some obvious difference between the experimental set-ups. When we removed the proventricle region (cutting site 2), we could observe that in the posterior end the stolonization is accelerated; only few segments and the pygidium were regenerated after stolonization;  usually only male stolons were produced; and, most interestingly, the appearance of aberrant stolons (Fig. 4). These aberrant stolons showed a great variety of segment number and order . Some of them were even composed of several sequential stolons, which differed in development. In one case, the anterior end appeared to be a composition of two segments with a total of 11 eyes, three antennae but only one parapodium. That such “monsters” can be actually experimentally induced carries a huge potential for evodevo studies.

monster

Fig. 4: Aberrant stolon developed after the removal of the proventicle region.

Obviously, removal of the proventricle region has a strong effect on stolonization and posterior regeneration. These results are in agreement with previous studies (e.g., Franke 1980, Heacox and Schroeder 1982) and clearly support an regulatory function of this region. However, it is difficult to really pinpoint the function to the proventricle, as we removed the complete region containing it. Other authors only removed the proventricle (by extirpation), but even in this case its likely that for example surroundig nervous system tissue will be damaged. We investigated proventricle morphology (Fig. 5) and found no hints suggesting an endocrine function of this organ. The proventricle of syllids is basically a muscle structure, composed of large sarcomeres and granules with high amounts of phosphorus and especially calcium ions. Our histological survey has revealed that there is no obvious of glandular tissue through the whole proventricular area. However, if the control of the stolonization process is really mediated by hormones, the surrounding nervous system might be a candidate, as they could release neuropeptides. Such peptides have been shown to control life-phase transitions and behaviour in Platynereis. Future experiments focussing on these hormons might help to unravel how the process of stolonization is controlled in syllids.

proventricle

Fig. 5: Histological section of the proventricle region

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