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Evolutionary integration of forelimb and hindlimb proportions within the bat wing membrane inhibits ecological adaptation
Nature Ecology & Evolution ( IF 13.9 ) Pub Date : 2024-11-01 , DOI: 10.1038/s41559-024-02572-9
Andrew Orkney, David B. Boerma, Brandon P. Hedrick

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.



中文翻译:


蝙蝠翅膜内前肢和后肢比例的进化整合抑制了生态适应



蝙蝠和鸟类由它们的飞行趋同进化来定义,假设需要翅膀和腿进化的模块化解耦。尽管有大量证据支持鸟类的这种解释,但还没有系统地尝试识别蝙蝠肢体骨骼中的模块化组织。在这里,我们展示了来自 111 种现存蝙蝠物种的系统发育代表性和生态多样性的肢体骨骼测量集合。我们将此数据集与 149 种鸟类的纲要进行了比较,这些鸟类已知表现出模块化进化和解剖学区域化骨骼适应。我们证明,与鸟类相比,冠蝠的形态多样性与前肢和后肢内部和之间的强烈性状整合有关。蝙蝠肢体骨骼的不同区域适应了不同生态活动的变化,飞行式的变化通过远端翅膀的适应来适应,而拇指和后肢在促进对栖息习惯变化的适应性反应方面发挥着重要作用。我们认为翼膜在整个蝙蝠骨骼中强制执行进化整合,强调蝙蝠拇指的进化与其他肢体骨骼比例的进化相关性较低。我们提出强烈的肢体整合抑制了蝙蝠的适应性反应,解释了与鸟类相比,它们的表型进化率较低,进化动力学相对同质。因此,由膜翼实现的动力飞行不仅是蝙蝠的一项关键创新,而且是它们的决定性抑制。

更新日期:2024-11-01
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