Andrew Orkney, David B. Boerma, Brandon P. Hedrick
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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.</p>","PeriodicalId":18835,"journal":{"name":"Nature ecology & evolution","volume":null,"pages":null},"PeriodicalIF":13.9000,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Evolutionary integration of forelimb and hindlimb proportions within the bat wing membrane inhibits ecological adaptation\",\"authors\":\"Andrew Orkney, David B. Boerma, Brandon P. Hedrick\",\"doi\":\"10.1038/s41559-024-02572-9\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>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.</p>\",\"PeriodicalId\":18835,\"journal\":{\"name\":\"Nature ecology & evolution\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":13.9000,\"publicationDate\":\"2024-11-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Nature ecology & evolution\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1038/s41559-024-02572-9\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"ECOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Nature ecology & evolution","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1038/s41559-024-02572-9","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
Evolutionary integration of forelimb and hindlimb proportions within the bat wing membrane inhibits ecological adaptation
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.
Nature ecology & evolutionAgricultural and Biological Sciences-Ecology, Evolution, Behavior and Systematics
CiteScore
22.20
自引率
2.40%
发文量
282
期刊介绍:
Nature Ecology & Evolution is interested in the full spectrum of ecological and evolutionary biology, encompassing approaches at the molecular, organismal, population, community and ecosystem levels, as well as relevant parts of the social sciences. Nature Ecology & Evolution provides a place where all researchers and policymakers interested in all aspects of life's diversity can come together to learn about the most accomplished and significant advances in the field and to discuss topical issues. An online-only monthly journal, our broad scope ensures that the research published reaches the widest possible audience of scientists.