Bone is a defining characteristic of the vertebrate skeleton, and while chondrichthyans (sharks, skates, and other cartilaginous fishes) are vertebrates, they are hypothesized to have lost the ability to make bone during their evolution. Multiple descriptions of a bone-like tissue in neural arches of vertebrae in various shark species (selachians), however, challenge this hypothesis. Here, we extend this argument by analyzing vertebrae of two members of the batoids (the little skate Leucoraja erinacea and Eaton's skate Bathyraja eatonii), the sister group to selachians within elasmobranchs. Micro-CT images showed a bone-like mineralization pattern in neural arches of each skate species, and histological analyses confirmed that this bone-like tissue surrounded a cartilage core, exactly as described in sharks. Another mineralization pattern identified in skate vertebrae was distinct from the polygonal tesseral and areolar patterns that classically are associated with the chondrichthyan endoskeleton. Many regions of the vertebrae, including the neural spine and transverse processes, showed this perichondral mineralization pattern, termed here trabecular tesseral. Other than the cartilage core of the neural arch, all mineralized tissues in skate vertebrae had flattened cells surrounded by matrix with bone-like histology. Analyses of quantitative microstructural parameters revealed that, compared to rat vertebrae, the bone-like mineralization pattern in the neural arches of skate vertebrae was more similar to compact bone than trabecular bone. In contrast, the thickness of the trabecular tesseral pattern was more similar to trabecular bone than compact bone of rat vertebrae. In conclusion, a bone-like tissue in neural arches of skate vertebrae appears to be a novel elasmobranch synapomorphy. We propose that the trabecular tesseral mineralization pattern in the skate might have deep homology to the mineralization pattern utilized in trabecular bone. STATEMENT OF SIGNIFICANCE: Mineralization patterns of skeletal tissues have not been investigated thoroughly in all vertebrate clades. Despite their designation as 'cartilaginous fish', chondrichthyans clearly evolved from ancestral vertebrates that made bone. The consensus that chondrichthyans lost the ability to make bone during their evolution, however, is challenged by reports of bone and bone-like tissues in the neural arches of vertebrae in extant sharks (selachians). Here, we provide evidence from micro-CT imaging and histological analyses to support our hypothesis that a bone-like tissue is present in the neural arches of batoids (the sister group to selachians within elasmobranchs). These results argue strongly that the neural arch bone-like tissue is a previously unknown synapomorphy of elasmobranchs. In addition to the bone-like mineralization pattern identified in the neural arches, micro-CT images also showed a novel mineralization pattern which we described as trabecular tesseral. Quantitative microstructural features shared between trabecular tesseral pattern and trabecular bone (from homologous rat vertebrae) suggest that both patterns might derive from an ancestral gene network driving trabecular mineralization (i.e., deep homology).

中文翻译：

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滑冰中的骨样特征提示一种新颖的弹枝突触和小梁矿化模式的深层同源性。

骨骼是脊椎动物骨骼的定义特征，而软骨鱼类（鲨鱼，滑冰鞋和其他软骨鱼类）是脊椎动物，但据推测它们在进化过程中丧失了制造骨骼的能力。但是，对各种鲨鱼物种（狼蛛）的椎神经弓中的骨样组织的多种描述对这一假设提出了挑战。在这里，我们通过分析两个蝙蝠类动物的椎骨（小溜冰鞋Leucoraja erinacea和伊顿的溜冰鞋Bathyraja eatonii）来扩展这一论点，这是一群在弹性支中的slachians的姐妹。Micro-CT图像显示了每种滑冰物种的神经弓中的骨样矿化模式，组织学分析证实，这种骨样组织完全围绕着鲨鱼的软骨。滑冰椎骨中发现的另一种矿化模式与传统上与软骨鱼类内骨骼有关的多边形后齿和乳晕模式不同。椎骨的许多区域，包括神经脊柱和横突，都显示了这种软骨周围的矿化模式，在这里被称为小梁骨。除神经弓的软骨核心外，滑冰椎骨中所有矿化的组织都被扁平化的细胞所包围，并具有类似骨组织学的基质。定量的微结构参数分析表明，与大鼠椎骨相比，滑行椎骨神经弓中的骨样矿化模式更类似于紧密骨，而不是小梁骨。相比之下，小梁小腿骨图案的厚度与小梁骨相似，而不是大鼠椎骨的紧密骨。总之，滑冰椎骨神经弓中的骨样组织似乎是一种新颖的弹性分支突触。我们认为，滑冰中的小梁后路矿化模式可能与小梁骨中使用的矿化模式具有深远的同源性。意义声明：尚未对所有脊椎动物进化枝中的骨骼组织矿化模式进行彻底调查。尽管软骨鱼类被命名为“软骨鱼类”，但它们显然是从制造骨骼的祖先脊椎动物进化而来的。软骨鱼类在进化过程中丧失了制造骨骼的能力的共识是，对于现存鲨鱼（狼蛛）椎骨神经弓中的骨骼和类骨组织的报道提出了挑战。在这里，我们提供了来自微CT成像和组织学分析的证据，以支持我们的假设，即类蝙蝠的神经弓（弹性支中的slachians的姐妹组）的神经弓中存在骨样组织。这些结果强烈证明，神经弓骨样组织是弹性支的先前未知的突触。除了在神经弓中识别出的骨样矿化模式外，微型CT图像还显示了一种新颖的矿化模式，我们将其称为小梁胫骨。