Mayuko Nakamura (2nd Year Doctoral Student, Department of Biological Sciences)

Kohei Oguchi (Doctoral student, Graduate School of Science, at the time of research)

Shojihito Omori (Assistant Professor, Niigata University)

Hisanori KOUZUKA (Technical Specialist, Misaki Marine Biological Station)

Masashi Ise (Postdoctoral researcher, University of the Ryukyus)

Naoto Jimi (Assistant Professor, Nagoya University)

Toru Miura (Professor, Misaki Marine Biological Station)

 

Key points of the presentation

• Through a diving survey in the waters around Sado Island, we discovered a new annelid with a diverging body ^{(Note 1)} and named it King Giedrasilis ^{(Note 2} ).
• It is extremely rare to find a left-right homologous animal with a branched torso system. The body of this species branches many times toward the tail, stretching in all directions within the host caemen ^{(Note 3} ).
• The discovery of King Giedrasilis, which is of great evolutionary and embryological interest, may also provide clues to the evolutionary process of left-right homologous animal morphology.

 

Summary of presentation

An international research team led by Professor Miura of the Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo, and Professor Aguado of the University of Göttingen, Germany, conducted a diving survey on Sado Island and collected an annelid with a peculiar system in which the body trunk diverges, coexisting within the sponges.

Observations of external morphology, internal organization, and ecology, as well as molecular phylogenetic analysis, revealed that this annelid is a new species in the genus Ramisyllis, and because of the diverging trunk, it was described as R. kingghidorahi, after the monster King Ghidorah.

The multiple branching toward the tail is thought to be an adaptation for efficiently absorbing nutrients and reproducing by distributing the body around the body of the host sponges. This finding suggests that there are still organisms in the seas around Japan that deviate from the conventional biological knowledge, and may contribute greatly to the future development of marine biology.

 

Contents of Presentation

Background of Research
Left-right homologous animals have a left-right homologous regime for a single cephalic and caudal axis, and it is very rare for the cephalic and caudal axes to diverge in the normal developmental process. However, some annelid Siluridae were known to have divergent body axes. The most prominent is the calacanthus sylis Syllis ramosa, which was reported from Asian waters around the end of the 19th century and from the interior of deep-sea caimen at Misaki. More recently, Ramisyllis multicaudata, a sylis with divergent body axes, was reported from shallow waters near Darwin in northern Australia. This species differs from the Calaxacus sylis in host caimen species, habitat, and morphology, and exhibits a unique ecology in which swimming breeding individuals (stolons ^{(Note 4} )) are released from multiple tails to reproduce. Although only the above two species of cirripedes with divergent body axes have been reported, a new species of Ramisyllis was discovered in the shallow waters around Sado Island in the Sea of Japan.

 

Research Details
In October 2019, a team of researchers from the University of Tokyo, Misaki Marine Biological Station, Niigata University, Sado Marine Biological Station, the University of Göttingen, and the Autonomous University of Madrid conducted a diving survey in Shukunegi in the southern part of Sado Island and collected a caemen with the annelids living inside (Figure 1).

Figure 1: King Giedrasilis was collected in shallow water at Shukunegi, Sado Island (A, B). It inhabits the interior of a species of the genus Catadromous (C), which attaches to rocks at depths of more than 10 m. Numerous tails can be seen protruding from the body surface of the caecilian (D).

 

The collected individuals were observed in life, histologically, and immunostained, and DNA was further extracted and several genes were sequenced for molecular phylogenetic analysis, and the entire mitochondrial genome sequence was also determined. The results strongly suggest that this species from Sado Island is closely related to R. multicaudata from Australia, but is a separate species, so it is described as a new species as R. kingghidorahi. The numerous cilia in the digestive tract leading to the anal opening in the tail of this species suggest that it facilitates the inflow of seawater through the tail. The markedly divergent regime of this species (Figure 2) was shown to have the reproductive advantage of allowing the release of breeding individuals from numerous tails, as well as the possibility of a role in increasing nutrient absorption efficiency by taking in seawater from the tail.

Figure 2: The characteristic regime of King Giedrasilis. The head is single, branching toward the tail (A). The caudal end branches into many branches (B), and a stolon, a swimming-breeding individual, is often developed (C). The trunk of the body is also branched, including the digestive tract, nerves, and muscles (D). Stolons develop gonads in the body in either males or females. The photo shows a female (E).

 

Significance and Prospects
Animals with a pattern of body axis divergence are extremely interesting research subjects from an embryological perspective. However, once discovered from the seas around Japan, Karakusasiris has not been found in recent years, and research on such animals has been completely stagnant. The fact that King Giedrasiris has been collected from relatively accessible waters near Japan and its morphology has been described in detail is extremely important for clarifying the diverse morphology and ecology exhibited by the animal in the future. King Giedrasilis has an extremely odd morphology compared to common animals (Figure 2). By unraveling the ecology and physiological functions behind it, there is a strong possibility that the conventional wisdom of biology will be overturned. There are still many unresolved biological characteristics of this species, and it is hoped that the clarification of these characteristics will lead to new biological findings in the future.

 

Journal

Journal name	Organisms Diversity & Evolution
Title of paper	Ramisyllis kingghidorahi n. sp., a new branching annelid from Japan
Author(s)	M. Teresa Aguado*; Guillermo Ponz-Segrelles, Christopher J. Glasby, Rannyele P. Ribeiro, Mayuko Nakamura, Kohei Oguchi, Akihito Omori, Hisanori Kohtsuka, Christian Fisher, Yuji Ise, Naoto Jimi, Toru Miura
DOI Number	10.1007/s13127-021-00538-4
Abstract URL	https://link.springer.com/article/10.1007/s13127-021-00538-4

 

Terminology

Note 1: Annelids .

A group of invertebrates with elongate bodies separated by body segments. This group includes gorgonians such as sillis, earthworms, leeches, etc. ↑up

Note 2 Silis

A generic name for annelids belonging to the family Siluridae, a lineage of polychaetes such as gobies. They live in various marine areas and lead a benthic lifestyle. Some species show a special reproductive mode in which a part of the body becomes free to release sperm and eggs (see Note 4). ↑up

Note 3: Caecilians

A generic name for animals belonging to the phylum sponges. A stickleback that inhabits a wide range of marine areas. It is the oldest branching lineage in the animal kingdom, and although it is a multicellular animal, it does not show clear tissue differentiation. They take in seawater and food through small pores on their surface and expel it through openings called pores. They often cohabit with other animal species in the empty spaces inside their bodies. ↑up

Note 4: Swimming breeders (stolon)

In annelids of the family Cirrhidae, a part of the body with dense gonads swims separately as a breeding individual and reproduces sexually by releasing sperm and eggs. Swimming breeding individuals detached from the main body are called stolons. ↑up