The squirrel barrier concept and its bearing on the evolution of aerial mammals

Abstract Three vertebrate lineages conquered powered fight in different epochs of the Phanerozoic: pterosaurs, dinosaurs (birds) and mammals (bats). The evolutionary mechanisms proposed for the demanding transition to powered flight have been contentious. For mammals, recent evidence suggests that the Darwinian hypothesis of a gliding transition is supported, based on aerodynamic and paleo-atmosphere reconstructions. However, it is surprising that the many (at least 12) confirmed, independent lineages of gliding mammals that existed since the Jurassic to the present never evolved powered flight. To explain this, Pennycuick in 2008 advanced the theoretical concept of the squirrel barrier: gliding mammals face a tradeoff between the cost of abandoning their agile arboreal lifestyle, and the potential gains of powered flight, thereby limiting the evolution of the higher-aspect-ratio wings required for achieving the latter. This concept was seldom discussed, used or tested. Here we examine critically the squirrel barrier concept and its implicit components, contrasting its predictions with available evidence, specifically from morphology, aerodynamics, and fossils. We found the concept highly relevant, and more complex than originally stated. A more nuanced approach to the probable conditions that must be met to transition from the locomotor style of ancestors to flying descendants reveals several intermediate such barriers, of which the squirrel barrier is one requiring profound evolutionary changes. Glide distance is a measure of glide efficiency, because the longer the glide the better the use of the large amount of energy invested in climbing up to the launch point in the canopy. Based on observational data and aerodynamics, we hypothesize that colugos (Dermoptera: Cynocephalidae) are able to maximize glide distance and glide ratio beyond average performance and thus might be beyond the squirrel barrier as proposed by Pennycuick, but still falling too short of reaching sustained powered flight, which constitute an additional, “hard” flight barrier.