The ovary organization in the marine limnodriloidin Thalassodrilides cf. briani (Annelida: Clitellata: Naididae) resembles the ovary of freshwater tubificins
Introduction
Thalassodrilides cf. briani is a marine species that has been recorded in two areas in Japan, i.e. the gravelly sand sediments of the subtidal zone in the Ehime Prefecture (Erséus, 1992) and the bottom sediments next to a fish farm in an embayment on the Pacific coast of southwestern Shikoku (Torii et al., 2016). The original description of T. briani comes from Hong Kong and with the exception of the shape of the copulatory sacs, it agrees with the Japanese specimens. However, due to the lack of genetic data for the Hong Kong population, the Japanese specimens are regarded as being conspecific with it (Torii et al., 2016). T. cf. briani was determined to be a suitable candidate for bioremediation processes due to its high potential to reduce the concentration of pollutants in marine sediments. T. cf. briani is able to efficiently convert 1-nitronaphthalene into nontoxic substances and it also degrades the polycyclic aromatic hydrocarbons in sediments (Ito et al., 2016a, Ito et al., 2016b). However, nothing is known about the sexual reproduction of this species, which could be important for its use on a large scale. Because of this lack of information, we decided to analyze as first the structure of the ovary and the course of oogenesis in this species.
Genus Thalassodrilides is a relatively small group of marine or brackish-water Naididae that are included into the subfamily Limnodriloidinae. Thalassodrilid species have been described from sediments in many localities in North America, China and Western Australia (Erséus, 1990; Milligan, 1996). Among the eight contemporary subfamilies that are included into the family Naididae i.e. Naidinae Ehrenberg, 1828; Pristininae Lastočkin, 1921; Opistocystinae Černosvitov, 1936; Tubificinae, Telmatodrilinae Eisen, 1879; Rhyacodrilinae Hrabě, 1963; Phallodrilinae Brinkhurst, 1971 and Limnodriloidinae Erséus, 1982 (Erséus et al., 2008, 2010a), the ovary organization and the process of egg formation have only been studied in detail in two of them – Naidinae and Tubificinae (Urbisz et al., 2010, 2015; Gorgoń et al., 2017). In both cases, the representatives that were studied were freshwater specimens. What is interesting is that the analysis revealed two substantially different types of ovaries: 1) in the representative of Naidinae (Stylaria lacustris) that was studied, the tiny ovaries only consist of a few syncytial germ-cell clusters (the so-called germ-line cysts), the cysts are made up of about 30 cells and detach quickly from the gonad and the majority of oogenesis occurs within the body cavity (Gorgoń et al., 2017); 2) in contrast, in Tubifex tubifex and other representatives of Tubificinae that have been studied, the conically shaped ovaries are composed of multicellular germ-line cysts (e.g. one huge cyst with as many as 2000 germ cells in a single ovary in T. tubifex) and the majority of oogenesis occurs within the gonad and only the vitellogenic oocytes detach from the ovary into the coelom (Urbisz et al., 2010, 2015).
It should be mentioned here that recent studies on the morphology, structure (cellular composition) and functioning of ovaries have revealed a great deal of plasticity among different clitellate taxa and that several types of ovaries have been distinguished (for details see Urbisz and Świątek, 2013; Gorgoń et al., 2017; Urbisz et al., 2017; see also Discussion). However, it seems that on the family/subfamily level, the morphology and structure of ovaries are conserved characters (Świątek et al., 2018). On the other hand, irrespective of their different morphology, the ovaries in clitellate annelids are always composed of syncytial cysts of germ cells that have a common architecture (with only one known exception – Capilloventer australis – for details see Discussion). In these types of cysts, each germ cell is connected to a common cytoplasmic mass, the cytophore, via one cytoplasmic bridge. Some characters that are connected with the morphology and structure of ovaries as well as the course of oogenesis seem to be helpful in determining the phylogenetic relationships between clitellates as was recently shown in leeches (Bielecki et al., 2014).
In the study presented here, we analyzed the organization of ovaries in a marine representative of Naididae – the limnodriloidin T. cf. briani and we compared it to the ovary structure and oogenesis that is known from freshwater Naididae and others clitellate annelids. Our studies revealed that the ovaries in T. cf. briani are small and elongated structures in which all germ cells are consolidated into one syncytial cyst. The developmental gradient of germ cells occurs along the long ovary axis. During oogenesis, the germ cells that are interconnected into cysts differentiate their fates and develop into oocytes and nurse cells. Only the oocytes develop into future egg cells and their growth, organelle accumulation and nutritive material uptake occur within the gonad.
T. cf. briani ovaries and the course of oogenesis strongly resembles that of the ovaries that are found in freshwater tubificin naidids. These results firmly support the concept of sister-group relations between Tubificinae and Limnodriloidinae as was previously suggested in studies on DNA sequences and morphological characters (Erséus et al., 2000; Marotta et al., 2003, 2008; Sjölin et al., 2005).
Section snippets
Animal material
Specimens of T. cf. briani were collected from the sediment in an embayment on the Pacific coast of southwestern Shikoku, Japan in 2016. Twenty sexually mature specimens were used for the study.
Light and transmission electron microscope analysis
Individuals were fixed with 2.5% glutaraldehyde in a 0.1 M phosphate buffer (pH 7.4) for several days. Whole specimens were observed using an Olympus SZ61TR stereomicroscope. Then, the region of the clitellum and several further body segments that contain the gonads and mature oocytes were sectioned and
General ovary organization
The ovaries in T. cf. briani are paired, small and inconspicuous structures that are located in the clitellum region on the ventral side of the body segment behind the segment with the testis. The individual ovary is slightly elongated in shape with a narrower proximal and broader distal section (Figs. 1B–D; 4). The proximal ovary tip is connected to the intersegmental septum by a thin ligament composed of somatic cells (Figs. 1B; 3A). The rest of the ovary lies in the body cavity between the
Ovary in T. cf. briani in comparison with other clitellate annelids
Ovarian morphology of clitellate annelids was on the focus of attention for many years. Older studies, however, based mainly on light microscopic observations concerned the localization of female gonad, their shape (general morphology) and the process of egg formation (Beddard, 1895; Michaelsen, 1928; Stephenson, 1930; see also references in Chapter 13 in Jamieson, 1981). Our knowledge in this field has increased significantly in recent years when the newly obtained data based on electron
Conclusions
Data presented here are the first report devoted to selected aspects of reproduction in limnodriloidin T. cf. briani. We have shown that the structure of T. cf. briani ovary strongly resembles 'Tubifex type' supporting the idea of sister relations of Limnodriloidinae and Tubificinae. We believe that for comparative purposes some characters relating to ovary structure and oogenesis may contribute to a better understanding of evolutionary changes in clitellate ovaries. To be able to accomplish it
Acknowledgements
Sincere thanks are due to Prof. Piotr Świątek (University of Silesia in Katowice, Poland) for his important discussion, useful corrections and suggestions. Authors are also grateful to Dr. Karol Małota (University of Silesia in Katowice, Poland) for his invaluable assistance in creating a three-dimensional reconstruction of the ovary.
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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