Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Evolutionary integration of forelimb and hindlimb proportions within the bat wing membrane inhibits ecological adaptation

Nature Ecology & Evolution volume 9, pages 111–123 (2025)Cite this article

Subjects

Abstract

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.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Bird wings and legs evolve independently, while bat wing and leg proportions are integrated.
Fig. 2: Bat thumb length varies more independently than any other skeletal element.
Fig. 3: Anatomically regionalized ecological adaptation across the bird and bat skeleton.
Fig. 4: Diversification of bird and bat gross limb proportions.

Similar content being viewed by others

Data availability

All original µCT scan data are available on MorphoSource. A CSV file of metadata and accompanying MorphoSource URLs for each specimen is available at Zenodo82 for the GitHub repository https://github.com/aorkney/Bats_n_Birds. This repository contains a précis of limb landmark constellations across the subject bats—prepared as .RData files—ecological scores and an associated BibTeX repository. Where dependent datasets such as phylogenies and bird landmark constellations are already available in public repositories, DOIs are provided to the original sources. The ‘README’ direction file provides detailed instructions for reproduction.

Code availability

A Zenodo release82 of the GitHub repository https://github.com/aorkney/Bats_n_Birds contains R scripts necessary to reproduce the main manuscript figures. These scripts are commented, including machine specifications, associated run-times and a detailed ‘README’ suite of instructions is provided.

References

  1. Wilson, D. E. & Reeder, D. M. Mammal Species of the World: A Taxonomic and Geographic Reference Vol. 1 (JHU Press, 2005).

  2. Upham, N., Esselstyn, J. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 17, e3000494 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Clements, J. et al. The eBird/Clements Checklist of Birds of the World: v2023 (Cornell Lab, 2023); www.birds.cornell.edu/clementschecklist/download/2023

  4. Simmons, N. & Cirranello, A. Bat Species of the World: A Taxonomic and Geographic Database. Version 1.4 (American Museum of Natural History, 2023); https://batnames.org/home.html

  5. Gill, F. B. Ornithology (Macmillan, 1995).

  6. Fenton, M. B. & Simmons, N. B. Bats: A World of Science and Mystery (University of Chicago Press, 2020).

  7. Nowak, R. M. & Walker, E. P. Walker’s Bats of the World (JHU Press, 1994).

  8. Wilman, H. et al. Eltontraits 1.0: species-level foraging attributes of the world’s birds and mammals: ecological archives e095-178. Ecology 95, 2027 (2014).

    Google Scholar 

  9. Ostrom, J. H. Archaeopteryx and the origin of flight. Q. Rev. Biol. 49, 27–47 (1974).

    Google Scholar 

  10. Pennycuick, C. On the reconstruction of pterosaurs and their manner of flight, with notes on vortex wakes. Biol. Rev. 63, 299–331 (1988).

    Google Scholar 

  11. McGuire, J. A. & Dudley, R. The biology of gliding in flying lizards (genus Draco) and their fossil and extant analogs. Integr. Comp. Biol. 51, 983–990 (2011).

    PubMed  Google Scholar 

  12. Wang, M., O’Connor, J. K., Xu, X. & Zhou, Z. A new Jurassic scansoriopterygid and the loss of membranous wings in theropod dinosaurs. Nature 569, 256–259 (2019).

    CAS  PubMed  Google Scholar 

  13. Gunnell, G. & Simmons, N. Fossil evidence and the origin of bats. J. Mammal. Evol. 12, 209–246 (2005).

    Google Scholar 

  14. Simmons, N. B., Seymour, K. L. & and G. F. Gunnell, J. Habersetzer Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821 (2008).

    CAS  PubMed  Google Scholar 

  15. Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996).

    PubMed  Google Scholar 

  16. Hallgrímsson, B., Willmore, K. & Hall, B. K. Canalization, developmental stability, and morphological integration in primate limbs. Am. J. Phys. Anthropol. 119, 131–158 (2002).

    Google Scholar 

  17. Bell, E., Andres, B. & Goswami, A. Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. J. Evol. Biol. 24, 2586–2599 (2011).

    CAS  PubMed  Google Scholar 

  18. Wagner, G. P. & Altenberg, L. Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).

    PubMed  Google Scholar 

  19. Young, N. M. & Hallgrímsson, B. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59, 2691–2704 (2005).

    PubMed  Google Scholar 

  20. Wein, A. & Schwing, R. Claws on the wings of kea parrots (Nestor notabilis). Notornis 64, 31–33 (2017).

    Google Scholar 

  21. Wagner, G. P., Pavlicev, M. & Cheverud, J. M. The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).

    CAS  PubMed  Google Scholar 

  22. Goswami, A., Smaers, J. B., Soligo, C. & Polly, P. D. The macroevolutionary consequences of phenotypic integration: from development to deep time. Phil. Trans. R. Soc. B 369, 20130254 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Zelditch, M. L. & Goswami, A. What does modularity mean? Evol. Dev. 23, 377–403 (2021).

    PubMed  Google Scholar 

  24. Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).

    PubMed  PubMed Central  Google Scholar 

  25. Nudds, R. L. Wing-bone length allometry in birds. J. Avian Biol. 38, 515–519 (2007).

    Google Scholar 

  26. Benson, R. B. & Choiniere, J. N. Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proc. R. Soc. B 280, 20131780 (2013).

    PubMed  PubMed Central  Google Scholar 

  27. Orkney, A., Bjarnason, A., Tronrud, B. C. & Benson, R. B. Patterns of skeletal integration in birds reveal that adaptation of element shapes enables coordinated evolution between anatomical modules. Nat. Ecol. Evol. 5, 1250–1258 (2021).

  28. Navalón, G., Bjarnason, A., Griffiths, E. & Benson, R. B. Environmental signal in the evolutionary diversification of bird skeletons. Nature 611, 306–311 (2022).

    PubMed  Google Scholar 

  29. Sears, K. E. Molecular determinants of bat wing development. Cells Tissues Organs 187, 6–12 (2007).

    PubMed  Google Scholar 

  30. Cooper, L. N., Cretekos, C. J. & Sears, K. E. The evolution and development of mammalian flight. WIREs Dev. Biol. 1, 773–779 (2012).

    CAS  Google Scholar 

  31. Varga, Z. & Varga, M. Gene expression changes during the evolution of the tetrapod limb. Biol. Futur. 73, 411–426 (2022).

    PubMed  Google Scholar 

  32. Boerma, D. B., Barrantes, J. P., Chung, C., Chaverri, G. & Swartz, S. M. Specialized landing maneuvers in Spix’s disk-winged bats (Thyroptera tricolor) reveal linkage between roosting ecology and landing biomechanics. J. Exp. Biol. 222, jeb204024 (2019).

    PubMed  Google Scholar 

  33. Adams, R. A. & Carter, R. T. Megachiropteran bats profoundly unique from microchiropterans in climbing and walking locomotion: evolutionary implications. PLoS ONE 12, e0185634 (2017).

    PubMed  PubMed Central  Google Scholar 

  34. López-Aguirre, C., Hand, S. J., Koyabu, D., Tu, V. T. & Wilson, L. A. Phylogeny and foraging behaviour shape modular morphological variation in bat humeri. J. Anat. 238, 1312–1329 (2021).

    PubMed  Google Scholar 

  35. Gaudioso, P. J., Martínez, J. J., Barquez, R. M. & Díaz, M. M. Evolution of scapula shape in several families of bats (Chiroptera, Mammalia). J. Zool. Syst. Evol. Res. 58, 1374–1394 (2020).

    Google Scholar 

  36. Hedrick, B. P. et al. Morphological diversification under high integration in a hyper diverse mammal clade. J. Mammal. Evol. 27, 563–575 (2020).

    Google Scholar 

  37. Arbour, J., Curtis, A. & Santana, S. Sensory adaptations reshaped intrinsic factors underlying morphological diversification in bats. BMC Biol. 19, 88 (2021).

  38. Rossoni, D. M., Patterson, B. D., Marroig, G., Cheverud, J. M. & Houle, D. The role of (co)variation in shaping the response to selection in the New World leaf-nosed bats. Am. Nat. 203, E107–E127 (2024).

  39. Hu, Y. et al. Evolution in an extreme environment: developmental biases and phenotypic integration in the adaptive radiation of antarctic notothenioids. BMC Evol. Biol. 16, 142 (2016).

  40. Rhoda, D. P., Haber, A. & Angielczyk, K. D. Diversification of the ruminant skull along an evolutionary line of least resistance. Sci. Adv. 9, eade8929 (2023).

    PubMed  PubMed Central  Google Scholar 

  41. Bjarnason, A. & Benson, R. A 3D geometric morphometric dataset quantifying skeletal variation in birds. MorphoMuseuM 7, e125 (2021).

  42. Pennycuick, C. The membrane wings of bats and pterosaurs. Theor. Ecol. Ser. 5, 135–160 (2008).

    Google Scholar 

  43. Cheney, J. A. et al. Hindlimb motion during steady flight of the lesser dog-faced fruit bat, Cynopterus brachyotis. PLoS ONE 9, e98093 (2014).

    PubMed  PubMed Central  Google Scholar 

  44. Zeller, R., López-Ríos, J. & Zuniga, A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 10, 845–858 (2009).

    CAS  PubMed  Google Scholar 

  45. Weatherbee, S. D., Behringer, R. R., Rasweiler IV, J. J. & Niswander, L. A. Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification. Proc. Natl Acad. Sci. 103, 15103–15107 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Adams, R. A. Evolutionary implications of developmental and functional integration in bat wings. J. Zool. 246, 165–174 (1998).

    Google Scholar 

  47. Murray, J. D., Maini, P. K. & Tranquillo, R. T. Mechanochemical models for generating biological pattern and form in development. Phys. Rep. 171, 59–84 (1988).

    Google Scholar 

  48. Unwin, D. M. Pterosaurs: back to the traditional model? Trends Ecol. Evol. 14, 263–268 (1999).

    CAS  PubMed  Google Scholar 

  49. Elgin, R. A., Hone, D. W. & Frey, E. The extent of the pterosaur flight membrane. Acta Palaeontol. Polon. 56, 99–111 (2011).

    Google Scholar 

  50. Lockley, M., Harris, J. D. & Mitchell, L. A global overview of pterosaur ichnology: tracksite distribution in space and time. Zitteliana 28, 185–198 (2008).

  51. Jagielska, N. & Brusatte, S. L. Pterosaurs. Curr. Biol. 31, R984–R989 (2021).

    CAS  PubMed  Google Scholar 

  52. Voigt, C. C., Borrisov, I. M. & Voigt-Heucke, S. L. Terrestrial locomotion imposes high metabolic requirements on bats. J. Exp. Biol. 215, 4340–4344 (2012).

    CAS  PubMed  Google Scholar 

  53. Boerma, D. B. & Swartz, S. M. Roosting ecology drives the evolution of diverse bat landing maneuvers. iScience 27, 110381 (2024).

  54. Vaughan, T. A. Functional Morphology of Three Bats: Eumops, Myotis, Macrotus (Univ. Kansas, 1959).

  55. Daniel, M. The New Zealand short-tailed bat, Mystacina tuberculata; a review of present knowledge. NZ J. Zool. 6, 357–370 (1979).

    Google Scholar 

  56. Bergou, A. J. et al. Falling with style: bats perform complex aerial rotations by adjusting wing inertia. PLoS Biol. 13, e1002297 (2015).

    PubMed  PubMed Central  Google Scholar 

  57. Riskin, D. K. et al. Bats go head-under-heels: the biomechanics of landing on a ceiling. J. Exp. Biol. 212, 945–953 (2009).

    PubMed  Google Scholar 

  58. Klingenberg, C. P. How exactly did the nose get that long? A critical rethinking of the Pinocchio effect and how shape changes relate to landmarks. Evol. Biol. 48, 115–127 (2021).

    Google Scholar 

  59. Adams, R. A. Morphogenesis in bat wings: linking development, evolution and ecology. Cells Tissues Organs 187, 13–23 (2007).

    Google Scholar 

  60. Stevens, R. D. & Guest, E. E. Wings of fringed fruit-eating bats (Artibeus fimbriatus) are highly integrated biological aerofoils from perspectives of secondary sexual dimorphism, allometry and modularity. Biol. J. Linn. Soc. 137, 711–719 (2022).

    Google Scholar 

  61. Shatkovska, O. & Ghazali, M. Relationship between developmental modes, flight styles, and wing morphology in birds. Eur. Zool. J. 84, 390–401 (2017).

    Google Scholar 

  62. Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1984).

  63. Middleton, K. M. & Gatesy, S. M. Theropod forelimb design and evolution. Zool. J. Linn. Soc. 128, 149–187 (2000).

    Google Scholar 

  64. Stanchak, K. E., Arbour, J. H. & Santana, S. E. Anatomical diversification of a skeletal novelty in bat feet. Evolution 73, 1591–1603 (2019).

    PubMed  Google Scholar 

  65. Simmons, N. B. & Geisler, J. H. Phylogenetic Relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to Extant Bat Lineages, With Comments on the Evolution of Echolocation and Foraging Strategies in Microchiroptera (American Museum of Natural History, 1998).

  66. Rietbergen, T. B. et al. The oldest known bat skeletons and their implications for Eocene chiropteran diversification. PLoS ONE 18, e0283505 (2023).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Shi, J. J. & Rabosky, D. L. Speciation dynamics during the global radiation of extant bats. Evolution 69, 1528–1545 (2015).

    PubMed  Google Scholar 

  68. Andres, B. The early evolutionary history and adaptive radiation of the Pterosauria. Acta Geol. Sin. 86, 1356–1365 (2012).

    Google Scholar 

  69. Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).

    CAS  PubMed  Google Scholar 

  70. Biewener, A. A. & Daley, M. A. Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control. J. Exp. Biol. 210, 2949–2960 (2007).

    PubMed  Google Scholar 

  71. Ijspeert, A. J. & Daley, M. A. Integration of feedforward and feedback control in the neuromechanics of vertebrate locomotion: a review of experimental, simulation and robotic studies. J. Exp. Biol. 226, jeb245784 (2023).

    PubMed  Google Scholar 

  72. Rothier, P. S., Fabre, A.-C., Clavel, J., Benson, R. B. & Herrel, A. Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity. eLife 12, e81492 (2023).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Weeks, P. Interactions between red-billed oxpeckers, Buphagus erythrorhynchus, and domestic cattle, Bos taurus, in Zimbabwe. Anim. Behav. 58, 1253–1259 (1999).

    CAS  PubMed  Google Scholar 

  74. Konishi, M. & Knudsen, E. I. The oilbird: hearing and echolocation. Science 204, 425–427 (1979).

    CAS  PubMed  Google Scholar 

  75. Woods, C. P., Czenze, Z. J. & Brigham, R. M. The avian “hibernation” enigma: thermoregulatory patterns and roost choice of the common poorwill. Oecologia 189, 47–53 (2019).

    PubMed  Google Scholar 

  76. Abourachid, A. et al. Hoatzin nestling locomotion: acquisition of quadrupedal limb coordination in birds. Sci. Adv. 5, eaat0787 (2019).

    PubMed  PubMed Central  Google Scholar 

  77. Horseman, N. D. & Buntin, J. D. Regulation of pigeon cropmilk secretion and parental behaviors by prolactin. Annu. Rev. Nutr. 15, 213–238 (1995).

    CAS  PubMed  Google Scholar 

  78. Hedrick, B. P. & Dumont, E. R. Putting the leaf-nosed bats in context: a geometric morphometric analysis of three of the largest families of bats. J. Mammal. 99, 1042–1054 (2018).

    Google Scholar 

  79. Jones, G. & Holderied, M. W. Bat echolocation calls: adaptation and convergent evolution. Proc. R. Soc. B 274, 905–912 (2007).

    PubMed  PubMed Central  Google Scholar 

  80. Adams, D., Collyer, M., Kaliontzopoulou, A. & Baken, E. Geomorph: software for geometric morphometric analyses. R package version 4.0.4. CRAN https://cran.r-project.org/package=geomorph (2022).

  81. Bookstein, F. L. Morphometric Tools for Landmark Data (Cambridge Univ. Press, 1997).

  82. Orkney, A. & Hedrick, B. P. aorkney/Bats_n_Birds: BatsnBirds, version 1.0.0. Zenodo https://doi.org/10.5281/zenodo.13742209 (2024).

  83. Scoones, J. C. & Hiscock, T. W. A dot-stripe Turing model of joint patterning in the tetrapod limb. Development 147, dev183699 (2020).

  84. Orkney, A. & Hedrick, B. P. Small body size is associated with increased evolutionary lability of wing skeleton proportions in birds. Nat. Commun. 15, 4208 (2024).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Findley, J. S., Studier, E. H. & Wilson, D. E. Morphologic properties of bat wings. J. Mammal. 53, 429–444 (1972).

    Google Scholar 

  86. Marinello, M. & Bernard, E. Wing morphology of neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Can. J. Zool. 92, 141–147 (2014).

    Google Scholar 

  87. Norberg, U. M. & Rayner, J. M. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Phil. Trans. R. Soc. B 316, 335–427 (1987).

    Google Scholar 

  88. Nebreda, S. M. et al. Disparity and macroevolutionary transformation of the Maniraptoran manus. Bull. Am. Mus. Nat. Hist. 440, 183–203 (2020).

    Google Scholar 

  89. Nudds, R., Dyke, G. J. & Rayner, J. Avian brachial index and wing kinematics: putting movement back into bones. J. Zool. 272, 218–226 (2007).

    Google Scholar 

  90. Hieronymus, T. L. Qualitative skeletal correlates of wing shape in extant birds (Aves: Neoaves). BMC Evol. Biol. 15, 30 (2015).

  91. Parr, C. S. et al. The Encyclopedia of Life v2: providing global access to knowledge about life on Earth. Biodivers. Data J. 2, e1079 (2014).

  92. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Google Scholar 

  93. Rohlf, F. J. & Corti, M. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753 (2000).

    CAS  PubMed  Google Scholar 

  94. Adams, D. C. & Collyer, M. L. On the comparison of the strength of morphological integration across morphometric datasets. Evolution 70, 2623–2631 (2016).

    PubMed  Google Scholar 

  95. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. cluster: cluster analysis basics and extensions, 2022. R package version 2.1.4. CRAN https://cran.r-project.org/package=cluster (2022).

  96. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).

  97. Pennell, M. et al. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216–2218 (2014).

    CAS  PubMed  Google Scholar 

  98. Clavel, J., Escarguel, G. & Merceron, G. mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Methods Ecol. Evol. 6, 1311–1319 (2015).

    Google Scholar 

Download references

Acknowledgements

We acknowledge the continued support of A. Bjarnason and R. Benson for their initial collection and distribution of the avian landmark constellations used in this study and B. Tronrud for the avian foot-use scores that she compiled in 2020. We acknowledge C. Goldstein for her diligent µCT data curation. We acknowledge the American Museum of Natural History, Cornell University Museum of Vertebrates, Harvard Museum of Comparative Zoology, University of Michigan Museum of Zoology, University of California Berkeley Museum of Vertebrate Zoology, Yale Peabody Museum, Muséum National d’Histoire Naturelle and Smithsonian National Museum of Natural History for use of bat µCT scan data generated from specimens housed in their collections. We acknowledge MorphoSource for curation and hosting of these data. We acknowledge the American Museum of Natural History, Cornell Institute of Biotechnology and Harvard University Center for Nanoscale Systems, for use of their biological imaging facilities. This manuscript is based upon work supported by the NSF Postdoctoral Research Fellowships in Biology Program under grant no. 1907235. The funders had no role in this project’s development, design and delivery. This funding applies to the work of D.B.B. Work undertaken by B.P.H. and A.O. was performed in part at the Harvard University Center for Nanoscale Systems; a member of the National Nanotechnology Coordinated Infrastructure Network, which is supported by the National Science Foundation under NSF award no. ECCS-2025158.

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Department of Biomedical Sciences, Cornell University, Ithaca, NY, USA

    Andrew Orkney & Brandon P. Hedrick

  2. Department of Biology, Dyson College of Arts and Sciences, Pace University, New York, NY, USA

    David B. Boerma

  3. Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY, USA

    David B. Boerma

Authors
  1. Andrew Orkney
    View author publications

    Search author on:PubMed Google Scholar

  2. David B. Boerma
    View author publications

    Search author on:PubMed Google Scholar

  3. Brandon P. Hedrick
    View author publications

    Search author on:PubMed Google Scholar

Contributions

A.O. envisioned and designed this study, supplemented the initial scan data collection, produced landmark constellations, undertook ecological scoring, undertook analyses and produced visualizations. D.B.B. undertook the majority of initial scan data collection and contributed to study design. B.P.H. envisioned and designed the study, supplemented the initial scan data collection, supervised and parsed analyses. All authors contributed to the written content of the manuscript.

Corresponding authors

Correspondence to Andrew Orkney or Brandon P. Hedrick.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Thomas Dececchi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Topological distance.

Topological distance is quantified as the number of appendicular epiphyseal joints (indicated by white circles) that must be crossed to travel between two bones. (a) The distance of the humerus to radius is 1, (b) Two joints must be crossed to travel from the humerus to the femur. (c) a third step will reach the tibia. (d) The femur and tibia are separated by 1 step. Blue, pink, white and black routes represent journeys between wing bones, leg bones, serially homologous and non-homologous bones.

Extended Data Fig. 2 Sex and age restricted cohorts replicate results.

(a) Normalized effect sizes of evolutionary covariances between bat skeletal element proportions. n=97 confirmed adults. (b) Normalized effect sizes of evolutionary covariances in random subsamples of 40 bat taxa, from a total of n=97 confirmed adults, organized by topological distance. n=40; 100 replicates. (c) Normalized effect sizes of evolutionary covariances between bat skeletal element proportions. n=47 males. (d) Normalized effect sizes of evolutionary covariances in random subsamples of 40 bat taxa, from a total of n=47 males, organized by topological distance. A decline in \(Z/\,\sqrt[]{n}\) with distance indicates a trend for more closely situated skeletal elements to exhibit stronger evolutionary integration n=40; 100 replicates. Grey envelope indicates the 95% confidence interval of n=40; 100 replicates from the full dataset of 111 species.

Extended Data Fig. 3 Phylograms of flight-style and foot-use across birds and bats.

(a) Flight-style variety across bats (b) Roosting ecology across bats (c) Flight-style variety across birds (d) Foot-use variety across birds. n bats =111, n birds =149.

Extended Data Fig. 4 Landmarking schemes employed to infer relative bat skeletal element sizes (Aethalops alecto used as model).

Landmarking schemes employed to infer relative bat skeletal element sizes: (a) Humerus (b) Handwing (c) Tibia (d) Radius (e) Femur, scale bar 10 mm (f) Schematic illustration of bat wing with handwing dactyl elements labelled mediolaterally I-V, and proximodistally a-d (g) Representation of variables included in handwing proportions, which are collapsed by Procrustes alignment and compiled into a 1 by 18 by n=111 array. (h) Representation of gross wing proportions, defined by the total wing length, craniocaudal depth and thumb length. This dataset is an n=111 by 3 table.

Extended Data Fig. 5 Removal of thumb landmarks affects perceived ecological adaptation within the bat wing.

(a) Normalized effect size of integration between transformed roosting ecology, bat gross wing proportions, handwing proportions, and the allometric residual of handwing size. Black: results when thumb landmarks are removed. (b) Normalized effect size of integration between transformed flight-style variety and bat morphological parameters. Effect-sizes computed within 100 randomly generated cohorts of n=100 bat species. Total available specimens n=111 bat species. The \(Z/\,\sqrt[]{n}=0.17\) isopleth (dashed) typically represents the lower bound of significance at an α=0.05 level. Solid envelopes represent significant relationships at the α=0.05 level, while dotted lines indicate non-significance. Illustrations A.O. 2024.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orkney, A., Boerma, D.B. & Hedrick, B.P. Evolutionary integration of forelimb and hindlimb proportions within the bat wing membrane inhibits ecological adaptation. Nat Ecol Evol 9, 111–123 (2025). https://doi.org/10.1038/s41559-024-02572-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41559-024-02572-9

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing