Y. Yamaguchi (Second-year student, Master's Program, Department of Biological Sciences)

Masato Hirose (Lecturer, School of Marine Life Science, Kitasato University)

Mayuko Nakamura (Department of Biological Sciences, 1st Year Doctoral Student)

Sumio Udagawa (Department of Biological Sciences, 2nd Year Doctoral Student)

Kohei Oguchi (Research Fellow, National Institute of Advanced Industrial Science and Technology)

Junpei SHINJI (Project Researcher, Research Center for Marine Education, Graduate School of Education)

Hisanori KOUZUKA (Technical Specialist, Misaki Marine Biological Station)

Toru Miura (Professor, Misaki Marine Biological Station)

Key points of the presentation

• In the archipelago ^{(Note 1)}, we have revealed for the first time the entire developmental process of an individual insect ^{(Note2) called the"bird's he} ad body (Note 3)," which is responsible for ^{defense in the archipelago (Note} 4).
• The observation of the developmental process of the bird's head body over time suggests that the bird's head body is derived from the evergreen insect ^{(Note 4)}.
• The elucidation of the mechanism for the establishment of the division of labor system in gregarious animals is expected to deepen our understanding of the evolution of sociality and individuality in animals.

Summary of presentation

The division of labor among individuals with different morphologies and behaviors in animal groups consisting of individuals of the same species is well known, as is caste differentiation in social insects. In group animals commonly found in marine environments, division of labor is known to occur within the same group, but it is unknown how individual worms with different morphologies (heteromorphic individual worms ^{(Note 5)} ) arise through the developmental process. It is particularly interesting to note that a wide variety of heteromorphic individual worms are found in moss worms, which are known as representative marine gastropods.

The research group led by Professor Toru Miura and graduate student Yu Yamaguchi of the Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo, used the Nagisa moss beetle, a species that is easy to collect and observe, to observe the developmental process of the "bird's head body" known as a defensive individual worm over time using scanning electron microscopy and tissue sections, and found three We found that the bird's head body is formed by three major budding processes. First, a cell mass that becomes the base peduncle cushion ^{(Note 6)} of the bird's head emerges from the tip of the everted insect, and from the base of the peduncle cushion, a protoplasm that forms the head (body of the bird's head) emerges. In addition, the tissue that will become the insect body ^{(Note 7)} buds from the inside of the head.

This study has established the basis for elucidating the developmental mechanism of heteromorphic individual insect differentiation in moss worms, and is expected to lead to an understanding of the evolutionary process of the division of labor system in group animals in the future.

Contents of presentation

Group animals live in "groups" in which individuals (individual worms) produced by clonal reproduction form groups while maintaining inter-tissue connectivity. In moss worms (ectoparasites), which are representative of clade animals, it is known that individual worms (heteromorphic worms) with very different morphologies arise within the same clade, sharing the same genome, and divide various functions (Figure 1).

Figure 1: Various morphologies of heteromorphic individual worms in moss worms. It is common for moss beetles to have multiple types of heteromorphic individual worms that sprout within the same group and divide the labor among them.

Among moss beetles, groups that sprout heteromorphic individuals and engage in division of labor are the most prosperous in the present life cycle, and the division of labor within a group is thought to have been important in enabling adaptation to diverse environments. Among the various heteromorphic individual worms, the "bird's head body," known as the defensive individual worm, is considered to be the most important individual worm found in most species. However, how the bird's head body arises and its developmental process is largely unknown.

A research group led by Professor Toru Miura and graduate student Yu Yamaguchi of the University of Tokyo clarified the developmental process of the bird's head body by temporal observation using the easily collected and easily observable species, the sandpiper Bugulina californica ( Figure 2).

Figure 2: Stereomicroscopic images of the Nagisa moss beetle (Bugulina californica ). (A) Overall view of the group. The evergreen insects form branches in rows, branching out to form a tufted colony. (B) Magnified image of a branch. The everbearing insects are spreading their tentacle crowns, and bird's-head bodies are sprouting from each everbearing insect. (C) Enlarged image of a bird's head. When it senses contact with a foreign body, it instantly closes its jaws and attacks.

To enable observation over time, we set up a rearing system in which groups of birds collected from outdoors are maintained in a tank in the laboratory. We observed the developmental process of the bird's head body every 8 hours and defined seven developmental stages (Figure 3).

Figure 3: Schematic diagram of the seven developmental stages of bird head bodies and the three major budding stages that occur during development.

Detailed observations using scanning electron microscopy and tissue sections at each developmental stage revealed that three major budding events occur during the development of the bird's head body.
(1) A cell mass, the peduncle cushion, emerges from the apical portion of the everted worm.
(2) From the peduncle cushion, the primordium that forms the head (the body of the bird's head) buds.
(3) In addition, the tissue that will become the body of the insect germinates inside the head.
The germination of the insect body is very similar to that of the insect body in ectoparasites, suggesting that the bird's head is formed by a modification of the developmental process of ectoparasites.

This study has established the basis for elucidating the developmental mechanism of heteromorphic individual insect differentiation in moss worms. In the future, we plan to elucidate more detailed developmental mechanisms, such as which genes are involved in the formation of the bird's head body. This is expected to lead to an understanding of the evolutionary process of the division of labor system, such as gregariousness and sociality.

Journal

Journal name	Zoological Science
Title of paper	Developmental process of a heterozooids: avicularium formation in a bryozoan, Bugulina californica
Author(s)	Haruka Yamaguchi, Masato Hirose, Mayuko Nakamura, Sumio Udagawa, Kohei Oguchi, Hisanori Kohtsuka, Toru Miura* (author)
DOI Number	https://doi.org/10.2108/zs200143

Terminology

Note 1: Community animals

A group of animals that increase their numbers through asexual reproduction such as division and budding, and that live as a group by linking individuals even after budding and division. Typical examples include moss worms, hydrozoans (cnidarians), and ascidians. ↑up

Note 2: Bird's head body

The bird's head has a form similar to a bird's beak, and when it senses contact with a foreign body (a small arthropod or other natural enemy animal), its jaws instantly close and it attacks. It is one type of atypical individual insect of moss beetles that specializes in defense against predators, and is so called because its morphology resembles the head of a bird. ↑ (up)

Note 3 Individual insect

The smallest unit that forms a group in a gregarious animal is called an individual insect. Individuals are called "individual worms" instead of "individuals" in group animals because they have various characteristics that are not found in "individuals" of single animals due to their organizational connections with other individual worms. ↑up

Note 4: Always an individual insect

The main individual insects of a clade, which feed by the crown of tentacles and have the ability to reproduce. ↑up

Note 5: Heteromorphic individual worms

Atypical individuals differ from normal individuals in that they lack feeding and reproductive capacities and are nourished by normal individuals connected by tissues. In addition to the bird's-head body mentioned in the text, other individual worms are known as heteromorphic individual worms, including the "empty individual worms" that support the swarm, the "egg chamber" that holds fertilized eggs until larval stages, and the "flagellum" that removes foreign substances from the swarm. ↑up

Note 6 peduncle cushion

A structure at the base of the bird's head body of the genus Bugulina, to which the Nagisa moss beetle belongs, and the closely related genus Bugula, which is filled with muscular tissue. ↑up

Note 7: Insect body

The outermost part of an individual moss animal is formed by a chitinous or calcareous cuticular layer (insect chamber), in which the tentacle crown, digestive tract, and muscles are housed. The part composed of those living cells is called the insect body. ↑ (up)