Skull diversity in the neotropical leaf-nosed bats (Phyllostomidae) evolved through a heterochronic process called peramorphosis, with underlying causes varying by subfamily. The nectar-eating (subfamily Glossophaginae) and blood-eating (subfamily Desmondontinae) groups originate from insect-eating ancestors and generate their uniquely shaped faces and skulls by extending the ancestral ontogenetic program, appending new developmental stages and demonstrating peramorphosis by hypermorphosis. However, the fruit-eating phyllostomids (subfamilies Carollinae and Stenodermatinae) adjust their craniofacial development by speeding up certain developmental processes, displaying peramorphosis by acceleration. We hypothesized that these two forms of peramorphosis detected by our morphometric studies could be explained by differential growth and investigated cell proliferation during craniofacial morphogenesis. We obtained cranial tissues from four wild-caught bat species representing a range of facial diversity and labeled mitotic cells using immunohistochemistry. During craniofacial development, all bats display a conserved spatiotemporal distribution of proliferative cells with distinguishable zones of elevated mitosis. These areas were identified as modules by the spatial distribution analysis. Ancestral state reconstruction of proliferation rates and patterns in the facial module between species provided support, and a degree of explanation, for the developmental mechanisms underlying the two models of peramorphosis. In the long-faced species, Glossophaga soricina, whose facial shape evolved by hypermorphosis, cell proliferation rate is maintained at lower levels and for a longer period of time compared to the outgroup species Miniopterus natalensis. In both species of studied short-faced fruit bats, Carollia perspicillata and Artibeus jamaicensis, which evolved under the acceleration model, cell proliferation rate is increased compared to the outgroup. This is the first study which links differential cellular proliferation and developmental modularity with heterochronic developmental changes, leading to the evolution of adaptive cranial diversity in an important group of mammals.

中文翻译：

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差异细胞增殖是叶口蝙蝠颅骨多样性异时生成的基础。


新热带叶鼻蝙蝠（Phyllostomidae）的头骨多样性是通过一种称为超态的异时过程进化而来的，其根本原因因亚科而异。食花蜜（舌咽亚科）和食血（Desmondontinae亚科）群体起源于食虫祖先，通过扩展祖先的个体发生程序、附加新的发育阶段并通过超态表现出超态，从而产生了独特形状的面部和头骨。然而，食果叶口动物（Carollinae 和 Stenodermatinae 亚科）通过加速某些发育过程来调整其颅面发育，通过加速表现出超态性。我们假设我们的形态测量研究检测到的这两种形式的超形态可以通过生长差异来解释，并研究了颅面形态发生过程中的细胞增殖。我们从四种野生捕获的蝙蝠物种中获取了代表一系列面部多样性的颅骨组织，并使用免疫组织化学标记了有丝分裂细胞。在颅面发育过程中，所有蝙蝠都表现出保守的增殖细胞时空分布，并具有明显的有丝分裂升高区域。通过空间分布分析将这些区域识别为模块。物种间面部模块增殖率和模式的祖先状态重建为两种超态模型的发育机制提供了支持和一定程度的解释。在长脸物种Glosssophaga soricina中，其面部形状是通过超形态进化而来的，与外群物种Miniopterus natalensis相比，细胞增殖率维持在较低水平且持续时间较长。 在所研究的两种短面果蝠中，Carollia perspicillata 和 Artibeus jamaicensis 在加速模型下进化，与外类群相比，细胞增殖率有所增加。这是第一项将差异性细胞增殖和发育模块性与异时发育变化联系起来的研究，导致重要哺乳动物群体适应性颅骨多样性的进化。