Integrative anatomical study of the branched annelid Ramisyllis multicaudata (Annelida, Syllidae)

Abstract

The sponge‐dwelling Syllidae Ramisyllis multicaudata and Syllis ramosa are the only annelid species for which a branched body with one head and multiple posterior ends is known. In these species, the head is located deep within the sponge, and the branches extend through the canal system of their host. The morphology of these creatures has captivated annelid biologists since they were first discovered in the late XIXth century, and their external characteristics have been well documented. However, how their branched bodies fit within their symbiotic host sponges and how branches translate into internal anatomy has not been documented before. These features are crucially relevant for understanding the body of these animals, and therefore, the aim of this study was to investigate these aspects. In order to assess these questions, live observation, as wells as histology, immunohistochemistry, micro‐computed tomography, and transmission electron microscopy techniques were used on specimens of R. multicaudata. By using these techniques, we show that the complex body of R. multicaudata specimens extends greatly through the canal system of their host sponges. We demonstrate that iterative external bifurcation of the body is accompanied by the bifurcation of the longitudinal organ systems that are characteristic of annelids. Additionally, we also highlight that the bifurcation process leaves an unmistakable fingerprint in the form of newly‐described “muscle bridges.” These structures theoretically allow one to distinguish original and derived branches at each bifurcation. Last, we characterize some of the internal anatomical features of the stolons (reproductive units) of R. multicaudata, particularly their nervous system. Here, we provide the first study of the internal anatomy of a branched annelid. This information is not only crucial to deepen our understanding of these animals and their biology, but it will also be key to inform future studies that try to explain how this morphology evolved.

Ramisyllis kingghidorahi n. sp., a new branching annelid from Japan

“…The three branching syllids show segmental asymmetry (i.e., segments with pairs of dorsal cirri of different length on each side), which intervenes between regions of symmetry (Schroeder et al, 2017) and have been found to show reddish coloration (Glasby et al, 2012;Imajima, 1966;Read, 2001). The glandular material of dorsal cirri in R. multicaudata changes from bright white into red colour when the animals start dying (Ponz-Segrelles et al, 2021), and we observed a similar phenomenon in R. kingghidorahi n. sp., with this material protruding through the dorsal cirri pores.…”

“…8h, i). Nevertheless, in both species, all longitudinal organs bifurcate in the branching points, new branches show internal muscular bridges crossing between the different organs and the ventral blood vessel is considerably enlarged in comparison with other syllids and similar in diameter to the digestive tube (Ponz-Segrelles et al, 2021).…”

“…11h, i); they form a "Y" shape (Fig. 11h, i,; Video S3), and appeared to be reduced as in R. multicaudata (Ponz-Segrelles et al, 2021), allowing the thinner digestive tube and ventral blood vessel to pass through them (Fig. 8h, i).…”

“…Seven specimens fixed in 90-100% ethanol and RNAlater were sequenced, together with seven specimens of R. multicaudata from Darwin (Australia) collected in 2009, 2015, and 2017 and fixed in RNAlater (Glasby et al, 2012;Ponz-Segrelles et al, 2021) (Table 1). Adequately fixed material is still not available for S. ramosa.…”

“…Remarks Ramisyllis kingghidorahi n. sp. and R. multicaudata (Glasby et al, 2012;Ponz-Segrelles et al, 2021;Schroeder et al, 2017) differ from S. ramosa (except the Red Sea and Imajima's 2005 Sagami Bay specimens) in living from 0 to 20-m depth inside species of Petrosia instead of 100-1000 m depth inside species of Crateromorpha (Izuka, 1912;McIntosh, 1879;Oka, 1895); in having the proliferating area after the parapodia and never replacing it or the dorsal cirri (Glasby et al, 2012) instead of new branches emerging from the parapodium and lacking dorsal cirri as in S. ramosa; in lacking two branches emerging from both sides of the same segment, which may occur in S. ramosa (Pl. XXIII, Fig.…”