150 million years of sustained increase in pterosaur flight efficiency

Abstract

The long-term accumulation of biodiversity has been punctuated by remarkable evolutionary transitions that allowed organisms to exploit new ecological opportunities. Mesozoic flying reptiles (the pterosaurs), which dominated the skies for more than 150 million years, were the product of one such transition. The ancestors of pterosaurs were small and probably bipedal early archosaurs1, which were certainly well-adapted to terrestrial locomotion. Pterosaurs diverged from dinosaur ancestors in the Early Triassic epoch (around 245 million years ago); however, the first fossils of pterosaurs are dated to 25 million years later, in the Late Triassic epoch. Therefore, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group. Here we describe the evolutionary dynamics of the adaptation of pterosaurs to a new method of locomotion. The earliest known pterosaurs took flight and subsequently appear to have become capable and efficient flyers. However, it seems clear that transitioning between forms of locomotion2,3—from terrestrial to volant—challenged early pterosaurs by imposing a high energetic burden, thus requiring flight to provide some offsetting fitness benefits. Using phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection that acted to increase flight efficiency over millions of years. Our results show that there was still considerable room for improvement in terms of efficiency after the appearance of flight. However, in the Azhdarchoidea4, a clade that exhibits gigantism, we test the hypothesis that there was a decreased reliance on flight5,6,7 and find evidence for reduced selection on flight efficiency in this clade. Our approach offers a blueprint to objectively study functional and energetic changes through geological time at a more nuanced level than has previously been possible.

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Fig. 1: Hypothesized scenarios of the evolutionary trajectory of flight performance metrics through time.
Fig. 2: Pterosaur phylogeny and the relationship of flight performance metrics with mass.
Fig. 3: Flight performance through time.

Data availability

The phylogeny that we generated in this study (Fig. 2a) is included as Supplementary Information (Supplementary Data 1) with this Article. No other data were generated or analysed during the current study. All data used are available from published sources and are cited in the text as appropriate.

Code availability

All analyses in this study were conducted using readily available, published programs and are cited in the text. Version numbers of the programs we used are as follows: Tracer v.1.7 (2018), MATLAB v.9.2 (2017), R v.3.4.4 (2017), BEAST 2 (2014) and BayesTraits v.3 (2018).

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Acknowledgements

We thank C. O’Donovan, M. Pagel, G. Ruxton and M. Sakamoto for discussions during the course of this study. J.B. was funded by the Leverhulme Trust (ECF-2017-22). C.V. was funded by a Leverhulme Trust Research Project Grant (RPG-2017-071). M.J.B. was funded by a Natural Environment Research Council (NERC) UK (grant NE/P013724/1) and European Research Council (ERC) Advanced Grant (number 788203).

Author information

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Authors

Contributions

C.V. and S.H. conceived the study. C.V., J.B., M.J.B. and S.H. collected the data. C.V., J.B., A.M. and S.H. conducted the phylogenetic and biophysical analyses. C.V., J.B., A.M., M.J.B. and S.H. interpreted the results and wrote the paper.

Corresponding authors

Correspondence to Chris Venditti or Stuart Humphries.

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The authors declare no competing interests.

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Peer review information Nature thanks Adrian Thomas and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Results of our n − 1 jack-knife procedure for the mass and wing area.

a, b, We compared the imputed values for each species from our phylogenetic imputation procedure with the published values for mass (a) and wing area (b), for studies in which that species had been excluded from the published value. Each point represents an individual species.

Extended Data Fig. 2 Comparison of flight performance metrics between pterosaurs and extant bats and birds.

a, We show the relationship between flight efficiency and mass in pterosaurs (Fig. 2b), with our mean phylogenetic imputations plotted with standard deviations shown as green ellipses. We superimpose a previously reported relationship between flight efficiency and mass for extant birds (orange line), as well as data points for six bat species (blue crosses). b, The relationship between sinking rate and mass for pterosaurs (Fig. 2c), with our mean phylogenetic imputations plotted with standard deviations shown by the blue ellipses. Superimposed, we show the range of the relationship between sinking rate and mass for Procellariiformes (orange box) and Accipitriformes7 (pink box) and individual data points for six specimens of an extinct Cretaceous bird (Sapeornis chaoyangensis) (orange circles with crosses), eleven extant bird species (orange crosses) and seven bat species (blue crosses). Triangles indicate pterosaur species for which we have published data on mass, wing area and wingspan. Circles indicate species for which we have only wingspan data. All azhdarchoids are coloured in red.

Supplementary information

Supplementary Information

This file contains Supplementary Text; Supplementary Table 1: Parameters for the flight model; and Supplementary Table 2: Species included in analyses (grey shading).

Reporting Summary

Supplementary Data 1

Posterior distribution of trees for pterosaurs produced from our phylogenetic inference model. File is provided in nexus format.

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Venditti, C., Baker, J., Benton, M.J. et al. 150 million years of sustained increase in pterosaur flight efficiency. Nature 587, 83–86 (2020). https://doi.org/10.1038/s41586-020-2858-8

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