Orkney Andrew, Boerma David B, Hedrick Brandon P
College of Veterinary Medicine, Department of Biomedical Sciences, Cornell University, Ithaca, NY, USA.
Department of Biology, Dyson College of Arts and Sciences, Pace University, New York, NY, USA.
Nat Ecol Evol. 2025 Jan;9(1):111-123. doi: 10.1038/s41559-024-02572-9. Epub 2024 Nov 1.
Bats and birds are defined by their convergent evolution of flight, hypothesized to require the modular decoupling of wing and leg evolution. Although a wealth of evidence supports this interpretation in birds, there has been no systematic attempt to identify modular organization in the bat limb skeleton. Here we present a phylogenetically representative and ecologically diverse collection of limb skeletal measurements from 111 extant bat species. We compare this dataset with a compendium of 149 bird species, known to exhibit modular evolution and anatomically regionalized skeletal adaptation. We demonstrate that, in contrast to birds, morphological diversification across crown bats is associated with strong trait integration both within and between the forelimb and hindlimb. Different regions of the bat limb skeleton adapt to accommodate variation in distinct ecological activities, with flight-style variety accommodated by adaptation of the distal wing, while the thumb and hindlimb play an important role facilitating adaptive responses to variation in roosting habits. We suggest that the wing membrane enforces evolutionary integration across the bat skeleton, highlighting that the evolution of the bat thumb is less correlated with the evolution of other limb bone proportions. We propose that strong limb integration inhibits bat adaptive responses, explaining their lower rates of phenotypic evolution and relatively homogeneous evolutionary dynamics in contrast to birds. Powered flight, enabled by the membranous wing, is therefore not only a key bat innovation but their defining inhibition.
蝙蝠和鸟类因其飞行的趋同进化而被定义，据推测这需要翅膀和腿部进化的模块化解耦。尽管有大量证据支持鸟类的这种解释，但尚未有系统的尝试来确定蝙蝠肢体骨骼中的模块化组织。在这里，我们展示了来自111种现存蝙蝠物种的具有系统发育代表性和生态多样性的肢体骨骼测量数据集。我们将这个数据集与149种鸟类的数据集进行比较，已知这些鸟类表现出模块化进化和解剖学上区域化的骨骼适应。我们证明，与鸟类不同，冠蝙蝠的形态多样化与前肢和后肢内部以及之间的强烈性状整合有关。蝙蝠肢体骨骼的不同区域适应以适应不同生态活动的变化，飞行方式的多样性通过远端翅膀的适应来实现，而拇指和后肢在促进对栖息习惯变化的适应性反应中发挥重要作用。我们认为翼膜加强了蝙蝠骨骼的进化整合，突出表明蝙蝠拇指的进化与其他肢体骨骼比例的进化相关性较小。我们提出，强烈的肢体整合抑制了蝙蝠的适应性反应，解释了它们与鸟类相比较低的表型进化速率和相对均匀的进化动态。因此，由膜状翅膀实现的动力飞行不仅是蝙蝠的一项关键创新，也是它们的决定性抑制因素。
