The internal bone structure in secondarily aquatic amniotes is modified from their terrestrial ancestries, as recognized as change in sectional compactness profile and bone density. The relationships between bone internal structure and mode of life have been documented in order to establish criteria for reconstructing the mode of life in extinct animals. However, the alternation in three-dimensional internal bone structure and its evolutionary process remains to be only partly understood.

In this study, in order to reveal how the internal limb bone structure of amniotes is modified in association with secondary aquatic adaptation, and to reveal what adaptive characteristics are seen in it, the author conducted a detailed comparison between amniotes living in a variety of environments ranging from dry land to deep sea. For clarification and functional interpretability of structures, the author uniquely categorizes lifestyle. The author focused especially on carnivorans (Mammalia: Carnivora) and turtles (Reptilia: Testudinata), which are promising materials to accomplish the purpose of this study in including plentiful terrestrial, semiaquatic, and aquatic members.

First, a novel method for two-dimensional comparison is established based on ontogenetic model. Since comparison using homologous sectional planes is necessary to discuss about evolutionary process, the author focused on the three-dimensional position of the center of ossification as a homologous point. Assuming that the position where a nutrient canal does not drift within compact bone, the center of ossification is estimated as the inferred origin of nutrient canal using three-dimensionally reconstructed CT data. The sagittal and transverse sectional planes are chosen as passing through the inferred center of ossification. These sectional images and three-dimensional translucent images are described microanatomically and compared interspecifically.

In carnivorans, the humeri of terrestrial taxa show tubular structure in diaphysis with open medullary cavity. In association with the secondary aquatic adaptation, the medullary region becomes filled with spongy bone and the periosteal compact bone is only locally thickened around the center of ossification. This condition is immediately interpreted as the inhibition of internal periosteal resorption in association with the reduction of cursoriarity. Among aquatic taxa, only Mirounga leonia shows an extremely spongy diaphysis, which is due to extensive resorption of periosteal compact bone. Epiphyseal and metaphyseal trabecular systems in terrestrial and semiaquatic taxa form orderly oriented architecture, whilst those of aquatic taxa show no preferred orientation.

In turtles, limb bone internal structure is characterized by lack of large open medullary cavity. Terrestrial taxa have tubular compact cortex in stylopodial diaphysis, although its internal region is filled with spongy bone. This pattern of internal limb bone structure is also found in a basal Testudinata Proganochelys quensteadti (Upper Triassic, Germany), whose lifestyle is believed to be terrestrial. In stylopodial and zeugopodial bones of semiaquatic to aquatic turtles, the spongy bone is restricted to the region of endochondral bone, resulting in local thickening of hourglass-shaped internal spongy bone. Humerus of a basal testudinate Mongolochelys efremovi (Late Cretaceous, Mongolia) with unknown lifestyle also follows this pattern. In Testudinata, Dermochelys coreacea have abundant spongy tissue in the region of periosteal origin. Unlike carnivoran mammals, architectural orientation of epi-/metaphyseal trabecular system does not occur in all terrestrial taxa.

The first common pattern found in the relationships between lifestyle in turtles and carnivorans, inhibited of periosteal resorption in semiaquatic to aquatic taxa compared to terrestrial taxa can be functionally interpreted as de-adaptation from terrestrial weight-bearing mode of life, in which the skeletal lightening saves the power required for locomotion. If the reduction of cavities is effective in body ballasting under water in these animals, it is more reasonable to reduce in bone resorption than adding more compact bone. On the other hand, the second common pattern, sponginess in periosteal bone in deep divers is interpreted as cancelation of the reduction in lung volume during diving. Since these ecological differences of three-dimensional internal bone structure depending on lifestyles is generalized among two phylogenetically independent tetrapod groups, it is claimable that the pattern of change in bone microanatomy is applicable for reconstruction of ecological evolution in completely extinct animal group, such as ichthyosaurs, plesiosaurs and desmostylians.

The higher compactness of limb bones in the terrestrial turtles compared to the terrestrial mammals suggests a weaker selection pressure for skeletal lightening, possibly due to the slow limb movements restricted by shells. Lack of architectural orientation of epi-/metaphyseal trabecular system in terrestrial turtles seems to occur also for the weak evolutionary selective pressure for constructing weight-bearing and stress-dispersing system with minimal bone mass.

本論文の論説部は四章からなる。第一章において、四足動物の骨内部構造が水棲適応進化に伴い劇的に変化することを示した。この現象を絶滅した動物の古生態復元に応用し、広く四足動物において起きた水棲適応進化の歴史を理解する上で、水棲適応と骨内部構造の関係を理解することの重要性を論じた。また、研究の目的として、(1)四足動物の二次的水棲適応に伴う骨内部の三次元構造の変化を正確に認識すること、及び(2)この変化を機能形態学的な視点から理解することの二点を明確化した。第二章では、CTを用いて取得した四肢骨の三次元データから、成長中心を通る断面の骨密度分布を記載し、その発達過程を推定する手法を開発したことを論じている。この手法を食肉類の上腕骨に適用した結果、陸棲種では骨端の骨梁骨と骨幹の髄腔が発達するが、半水棲種では髄腔の退縮が、水棲種では髄腔および骨梁骨の退縮が確認された。また深海潜水に適応した種では、骨の海綿質化が認められた。第三章においては、カメ類の四肢骨を用いて骨内部構造の種間比較を行った。カメ類の四肢骨には髄腔が発達せず、骨梁骨の発達には生態による顕著な差異は認められないことを記した。また陸棲種では、緻密骨が内部の再吸収により管状の構造をもつが、半水棲−水棲種においては緻密骨の管状化は起こらず、一部の深海潜水性のカメ類では骨内部が極端に海綿質化することが示された。第四章では、結果を踏まえ機能形態学的な視点から考察を行った。 カメ類では食肉類に比べ骨軽量化構造が発達しない傾向にあり、これは甲羅による四肢の運動の制限から、カメ類では骨軽量化を促す進化圧が低いことが示唆された。半水棲−水棲種における再吸収の抑制は、水棲適応に伴う軽量化構造からの脱適応として、深海潜水種の二次的な骨軽量化は肺の収縮時に遊泳効率を上げる適応として解釈できた。この二系統に共通する骨内部構造の進化パターンは、絶滅系統内での生態進化の復元に有効であることが推察された。末尾に謝辞と引用文献を備えている。

以下に評価を述べる。本論文は、動物学と古生物学の境界領域を繋ぐ、興味深い機能形態学的課題をテーマに選んだものである。カメ類と食肉類の多系統的比較から、骨組織の二次的水棲適応の解明という大きな問題点に切り込んだ、創造性に富む研究であるといえる。データ解析の緻密さ、論点の的確さ、論理性の厳格さ、そして考察において広く論議された進化形態学上の理論構築など、すべての点について世界最高水準の論文であると高く評価できる。構成する各章の内容それぞれも十分に吟味されたもので、抑制の効いた表現や慎重な言い回しなどを見ても、学界を説得する優れた作に仕上がっていると判断することができる。古生物学と動物行動学の議論を隔てなく貫き、三次元形態入力技法を解析と結び付けるなど、手法、解析、総合のそれぞれにおいて斬新で、これまでの論議を書き換えるに足る高度な説得力を具備している。

なお、本論文のとくに第二章、四章の一部は、遠藤秀紀、Alexander Houssayeとの共同研究であるが、論文提出者が主体となって分析及び検証を行ったもので、論文提出者の寄与が十分であると判断する。

したがって、博士(理学)の学位を授与できると認める。