Cytrynbaum Eli G, Small Clayton M, Kwon Ronald Y, Hung Boaz, Kent Danny, Yan Yi-Lin, Knope Matthew L, Bremiller Ruth A, Desvignes Thomas, Kimmel Charles B
Institute of Neuroscience University of Oregon Eugene Oregon 97403.
Institute of Ecology and Evolution University of Oregon Eugene Oregon 97403.
Evol Lett. 2019 Jul 16;3(4):374-391. doi: 10.1002/evl3.128. eCollection 2019 Aug.
The role of osteoblast placement in skeletal morphological variation is relatively well understood, but alternative developmental mechanisms affecting bone shape remain largely unknown. Specifically, very little attention has been paid to variation in later mineralization stages of intramembranous ossification as a driver of morphological diversity. We discover the occurrence of specific, sometimes large, regions of nonmineralized osteoid within bones that also contain mineralized tissue. We show through a variety of histological, molecular, and tomographic tests that this "extended" osteoid material is most likely nonmineralized bone matrix. This tissue type is a significant determinant of gill cover bone shape in the teleostean suborder Cottoidei. We demonstrate repeated evolution of extended osteoid in Cottoidei through ancestral state reconstruction and test for an association between extended osteoid variation and habitat differences among species. Through measurement of extended osteoid at various stages of gill cover development in species across the phylogeny, we gain insight into possible evolutionary developmental origins of the trait. We conclude that this fine-tuned developmental regulation of bone matrix mineralization reflects heterochrony at multiple biological levels and is a novel mechanism for the evolution of diversity in skeletal morphology. This research lays the groundwork for a new model in which to study bone mineralization and evolutionary developmental processes, particularly as they may relate to adaptation during a prominent evolutionary radiation of fishes.
成骨细胞定位在骨骼形态变异中的作用已得到较好理解，但影响骨骼形状的其他发育机制仍大多未知。具体而言，作为形态多样性驱动因素的膜内成骨后期矿化阶段的变异很少受到关注。我们发现骨骼中存在特定的、有时很大的未矿化类骨质区域，这些区域同时也含有矿化组织。我们通过各种组织学、分子和断层扫描测试表明，这种“扩展的”类骨质物质很可能是未矿化的骨基质。这种组织类型是硬骨鱼亚目杜父鱼亚目中鳃盖骨形状的一个重要决定因素。我们通过祖先状态重建证明了杜父鱼亚目中扩展类骨质的反复进化，并测试了扩展类骨质变异与物种间栖息地差异之间的关联。通过测量系统发育中不同物种鳃盖发育各阶段的扩展类骨质，我们深入了解了该性状可能的进化发育起源。我们得出结论，这种对骨基质矿化的精细发育调控反映了多个生物学层面的异时性，是骨骼形态多样性进化的一种新机制。这项研究为研究骨矿化和进化发育过程的新模型奠定了基础，特别是在鱼类显著进化辐射期间它们可能与适应相关的方面。
