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 over 150 million years (myr) were the product of one such transition. The ancestors of pterosaurs were small and likely bipedal early archosaurs1, which were certainly well adapted to terrestrial locomotion. Pterosaurs diverged from dinosaur ancestors in the Early Triassic (~245 myr ago, Ma), and yet their first fossils come 25 myr later, in the Late Triassic. Thus, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group. Our aim here is to study the evolutionary dynamics of pterosaurs’ adaptation to a new locomotory medium. 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 locomotion - from terrestrial to volant – challenged early pterosaurs by imposing a steep energetic hill to climb, thus requiring flight to provide some offsetting fitness benefits. Using novel phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection acting to increase flight efficiency over millions of years. Our results show that there was still significant room for improvement in terms of efficiency after the appearance of flight. However, in the Azdarchoidea, a clade exhibiting gigantism, we test the hypothesis that there was a decreased reliance on flight and find evidence for reduced selection on flight efficiency in this clade. By combining biophysical models and phylogenetic statistical methods with the fossil record, we offer a blueprint to study functional and energetic changes through geological time objectively at a far more nuanced level than has ever before been possible.