Collaborative Research: The role of multifunctionality in the evolution of cranial morphological diversity in bats

从昆虫的翅膀到鸟的喙，大多数解剖结构都有不止一种功能。解剖结构是如何进化来完成不止一种功能的，这是一个长期存在的重要问题。该项目通过研究头骨及其不同功能（如感知、呼吸和进食）如何相互作用来解决这个问题，并在进化过程中形成了头骨形态的多样性。为了研究这个主题，本项目将重点放在蝙蝠上，蝙蝠是哺乳动物中物种第二丰富的目，因为这个群体在物种数量上具有非凡的多样性，头骨形状和大小范围广泛，头骨功能新颖，如回声定位。为了了解头骨功能之间的相互作用如何帮助产生蝙蝠头骨多样性，研究人员将首先测量和绘制蝙蝠内部和外部头骨形态的多样性。然后，研究人员将使用计算模型和生理数据来预测和比较不同形状的头骨在进食、呼吸和嗅觉方面的表现，确定头骨的哪些部分影响这些功能以及如何影响这些功能。最后，研究人员将重建与功能相关的头骨特征是如何在竞争功能的背景下进化的。该项目将生成大量的头骨内部和外部形态学数据集（3D模型，组织学系列），使本科生和研究生的培训成为可能，并支持博物馆展览的发展，预计将在两个城市吸引数千名游客。揭示颅功能之间的性能关系和权衡的定量信息很少，这阻碍了对脊椎动物颅形态多样性形成因素的充分理解。该提案概述了一个高度整合的研究框架，该框架将明确地将形态学和性能多样性联系起来，跨越关键脊椎动物结构（头盖骨）的多种功能，从而增加对内在和外在因素哪些以及如何促进其形态进化的理解。该项目的中心假设是蝙蝠头盖骨的形态多样性是其功能之间结构、机械和生理相互作用的结果，包括权衡和促进。该项目将特别侧重于检查喙部（口部），因为它的形态和功能变化是大多数蝙蝠物种颅骨多样性的基础，以及在有限空间内保守和衍生的颅骨功能界面。该团队将采用综合和跨学科的方法来完成三个目标，并测试从主要假设得出的预测。在Aim 1中，该团队将使用微型计算机断层扫描（micro-CT）对蝙蝠头骨进行成像，并对内部和外部颅骨特征进行几何形态分析，以确定蝙蝠颅骨形态多样性的主要特征。在目标2中，该团队将使用选定蝙蝠物种的自然形态和改变形态模型进行测量、计算和计算建模，并验证：(1)将颅骨形态的变化转化为与蝙蝠生态相关的几个功能（进食、呼吸、嗅觉、视觉和回声定位）的性能输出，以及(2)确定性能关系和功能之间的权衡。在目标3中，该团队将使用系统发育比较分析来确定与功能相关的颅骨特征的进化模式，并检查折衷对形态多样性的影响。该项目将生成预测（有限元、计算流体动力学）模型，这些模型将得到实验验证，这将极大地推动生物力学领域的发展，并为未来旨在测量体内性能的研究奠定基础。通过在系统发育框架内结合描述和实验方法，该项目将是第一个明确解决多功能性在整个哺乳动物目的头盖骨形态多样化中的作用的项目。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

From insect wings to bird beaks, most anatomical structures carry out more than one function. How anatomical structures have evolved to accomplish more than one function is a long-standing, important question in the field of organismal biology. This project addresses this question by examining the skull and how its different functions – such as sensing, breathing, and feeding– interact and in so doing may have shaped the diversity of skull morphology over evolutionary time. To study this topic, this project focuses on bats, the second most species-rich Order of mammals, because this group offers extraordinary diversity in number of species, a wide range of skull shapes and sizes, and novel skull functions such as echolocation. To understand how the interaction among skull functions helped generate bat skull diversity, the researchers will first measure and map the diversity of internal and external skull morphology across bats. The researchers will then use computational models and physiological data to predict and compare how well differently shaped skulls perform during feeding, respiration, and olfaction, identifying what parts of the skull affect these functions and how. Finally, the researchers will reconstruct how functionally relevant skull features have evolved in the context of competing functions. The project will generate massive datasets of skull internal and external morphology (3D models, histological series), enable training of undergraduate and graduate students, and support the development of a museum exhibit projected to reach thousands of visitors across two cities.Quantitative information revealing the performance relationships and tradeoffs among cranial functions is scarce, which hinders a full understanding of the factors shaping cranial morphological diversity in vertebrates. This proposal outlines a highly integrative research framework that will explicitly link morphological and performance diversity across the multiple functions of a key vertebrate structure, the cranium, thereby increasing the understanding of which and how intrinsic and extrinsic factors contributed to its morphological evolution. This project’s central hypothesis is that the morphological diversity of the cranium of bats is the result of structural, mechanical, and physiological interactions among its functions, including tradeoffs and facilitation. The project will particularly focus on examining the rostrum (snout), because its morphological and functional variation underlies most of the cranial diversity across bat species, and conserved and derived cranial functions interface within its limited space. The team will use an integrative and cross-disciplinary approach to complete three aims and test predictions derived from the main hypothesis. In Aim 1, the team will use micro-Computed Tomography (micro-CT) to image bat skulls and geometric morphometric analyses of internal and external cranial features to identify the major traits that underlie cranial morphological diversity across bats. In Aim 2, the team will use models of natural and altered morphologies of selected bat species to conduct measurements, calculations, and computational modeling with validation to (1) translate variation in cranial morphology into performance outputs for several functions relevant to bat ecology (feeding, respiration, olfaction, vision and echolocation), and (2) identify performance relationships and tradeoffs among functions. In Aim 3, the team will use phylogenetic comparative analyses to identify patterns of evolution in functionally-relevant cranial traits, and examine the effect of tradeoffs on morphological diversity. The project will generate predictive (finite element, computational fluid dynamic) models that will be experimentally validated, which will greatly advance the field of biomechanics and serve as the basis for future studies aimed at measuring in vivo performance. By coupling descriptive and experimental approaches within a phylogenetic framework, the project will be the first to explicitly address the role of multifunctionality in the morphological diversification of the cranium across a whole mammalian Order.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.