Research
Our laboratory is interested in understanding the molecular genetic mechanisms of how vertebrates acquired novel structures during evolution. Our particular interest is to understand the fundamental body plan in relation to the formation of fins and limbs from an evolutionary perspective.
New Mechanism Uncovered for the Reduction of Emu Wings<br>~ The Lack of Muscle at the Distal Wings Leads to Bone Reduction and Asymmetry ~
The emu is a flightless bird with wings that have undergone significant reduction. Despite this, the precise mechanisms behind the morphological changes in their wings have remained largely unknown. In this study, we found that the emu wings not only show significant shortening, but the skeletal elements also fuse asymmetrically, a phenomenon traced back to the absence of muscle formation in the distal regions of the wings. During development, this lack of muscle leads to insufficient mechanical stress, which is crucial for proper bone formation. The team identified muscle progenitor cells with a unique dual identity, combining characteristics of both somite-derived myogenic and lateral plate mesoderm cells. These cells undergo cell death during muscle development, preventing the formation of distal muscles. The study highlights how differences in embryonic and fetal movement may play a pivotal role in driving morphological evolution, shedding light on the complex developmental processes that shape skeletal structures.
- Eriko Tsuboi*, Satomi F. Ono*, Ingrid Rosenburg Cordeiro*, Reiko Yu, Toru Kawanishi, Makoto Koizumi, Shuji Shigenobu, Guojun Sheng, Masataka Okabe, and Mikiko Tanaka(*These authors contributed equally to this work.)(2024). Immobilization secondary to cell death of muscle precursors with a dual transcriptional signature contributes to the emu wing skeletal pattern. Nature Communications 15, 8153.
Oxygen shapes arms and legs
The webbing between the fingers of some animals – the interdigital membranes – is formed in different ways across species. In collaboration with Dr. J. Hanken’s group (Harvard Univ.), we found that removal of the interdigital membrane by cell death depends on the production of reactive oxygen species, which only occurs in embryos exposed to a high oxygen concentration during development. This work gives an interesting example of how novel strategies to shape the body parts may appear during development, linking ecology and evolution of the limb shape.
- Ingrid Rosenburg Cordeiro, Kaori Kabashima, Haruki Ochi, Keijiro Munakata, Chika Nishimori, Mara Laslo, James Hanken, and Mikiko Tanaka(2019). Environmental oxygen exposure allows for the evolution of interdigital cell death in limb patterning. Developmental Cell 50, 155-166.
Basis of Development of Vertebrate Limb Muscles has been established in Cartilaginous Fishes
The development of limb muscle has been well studied in most land dwelling vertebrates such as humans and modern research models. In these species, muscle precursors, or cells that will form limb muscle, travel to the limb bud, a location in the developing embryo where they multiply and form muscle tissue under the control of genes that coordinate limb- muscle formation, such as Lbx1. It has been shown that this mechanism of development is shared with bony but not with cartilaginous fish. Using catshark embryos, we confirmed that Lbx1-positive cells are found in cartilaginous fish fin as well as in hypobranchial muscles, and that these are formed via the mechanism that has been established in land dwelling vertebrates as well as in bony fish.
- Eri Okamoto, Rie kusakabe, Shigehiro Kuraku, Susumu Hyodo, Alexandre Robert-Moreno, Koh Onimaru, James Sharpe, Shigeru Kuratani, Mikiko Tanaka(2017). Migratory appendicular muscles precursor cells in the common ancestor to all vertebrates. Nature Ecology & Evolution 1, 1731-1736.
Key genetic event underlying fin-to-limb evolution
The first four-legged, land-living creatures—known as early tetrapods—evolved from fish, following the transformation of fins into limbs. This fin-to-limb evolution is a crucial, yet so far unsolved, example of how morphological changes can dramatically alter life on Earth. In collaboration with Dr. J. Sharpe’s group (CRG), we have revealed how genetic alterations governing the patterning of skeletal structures in fins may have led to the evolution of limbs and the rise of early tetrapods.
- Koh Onimaru, Shigehiro Kuraku, Wataru Takagi, Susumu Hyodo, James Sharpe and Mikiko Tanaka(2015). A shift in anterior-posterior positional information underlies the fin-to-limb evolution. eLife 4, e07048.
- Koh Onimaru, Luciano Marcon, Marco Musy, Mikiko Tanaka and James Sharpe(2016). The fin to limb transition as the re-organisation of a Turing pattern. Nature Communications 7, Article number 11582.