School of Biological Sciences, The University of Adelaide, Adelaide, SA, Australia.
Department of Anatomy, Western University of Health Sciences, Pomona, CA, United States.
Evolution. 2023 Apr 1;77(4):1006-1018. doi: 10.1093/evolut/qpad020.
Biological variation is often considered in a scalable hierarchy, e.g., within the individual, within the populations, above the species level. Morphological integration, the concept of covariation among constituent parts of an organism, is also hierarchical; the degree to which these "modules" covary is a matter of the scale of the study as well as underlying processes driving the covariation. Multilevel analyses of trait covariation are a valuable tool to infer the origins and historical persistence of morphological diversity. Here, we investigate concordance in patterns of integration and modularity across three biological levels of variation: within a species, within two genera-level radiations, and among species at the family level. We demonstrate this approach using the skull of mammalian family Leporidae (rabbits and hares), which is morphologically diverse and has a rare-among-mammals functional signal of locomotion adaptation. We tested three alternative hypotheses of modularity; from the most supported we investigated disparity and integration of each module to infer which is most responsible for patterns of cranial variation across these levels, and whether variation is partitioned consistently across levels. We found a common pattern of modularity underlies leporid cranial diversity, though there is inconsistency across levels in each module's disparity and integration. The face module contributes the most to disparity at all levels, which we propose is facilitating evolutionary diversity in this clade. Therefore, the distinctive facial tilt of leporids is an adaptation to locomotory behavior facilitated by a modular system that allows lineages to respond differently to selection pressures.
生物变异通常被认为是一个可扩展的层次结构，例如在个体内部、种群内部、物种水平之上。形态整合，即生物体组成部分之间的协同变化的概念，也是分层的；这些“模块”协同变化的程度既是研究的尺度问题，也是驱动协同变化的潜在过程的问题。对特征协同变化的多层次分析是推断形态多样性的起源和历史延续的一种有价值的工具。在这里，我们研究了三个变异的生物学水平上的整合和模块性模式的一致性：在一个物种内、在两个属级辐射内以及在科水平的物种之间。我们使用哺乳动物科兔形目（兔子和野兔）的头骨来证明这种方法，兔形目头骨形态多样，具有哺乳动物中罕见的运动适应功能信号。我们测试了三种替代的模块性假设；从最支持的假设中，我们研究了每个模块的离散度和整合度，以推断哪个模块最负责这些水平上的颅骨变异模式，以及变异是否在各水平上一致地划分。我们发现，兔形目颅骨多样性的基础是一种共同的模块性模式，尽管每个模块的离散度和整合度在各水平上都不一致。面部模块对所有水平的离散度贡献最大，我们提出这是促进了这个分支的进化多样性。因此，兔形目的独特面部倾斜是一种对运动行为的适应，这是由一个允许谱系对选择压力做出不同反应的模块化系统促成的。
