The tail end of hummingbird evolution: parallel flight system development in living and ancient birds

Abstract

Evolutionary innovations are central to debates about biological uniformitarianism because their very novelty implies a distinct evolutionary dynamic. Traditional scenarios for innovations in the development of avian powered flight exemplify the kinds of distinctions considered to occur at different times during the history of innovations. Thus, the progressive change of the wing stroke mechanism early in its evolution is considered to have imposed strong functional and historical constraints on tail shape diversity, whereas attainment of the modern flight stroke mechanism is considered to have liberated the tail to radiate into a wide variety of other functions and forms. Detailed analyses of living hummingbirds revealed that these highly aerial birds actually expressed many parallel functional constraints and historically progressive patterns observed earlier in avian history: (1) more basal lineages had relatively weak wing muscles (patagial muscles and tendons, TPB), convex to square tails, and more linear flight employed in nonterritorial foraging; (2) more derived lineages had a stronger TPB, forked tails, accentuated growth of tail fork, and more manoeuvrable and agile flight employed in territorial foraging; and (3) the most derived lineage had the strongest TPB, greatly reduced tails, and mainly bee-like flight. These associations make functional sense because convex tails increase stability and efficiency in linear flight, concave tails augment lift for turning flight in territorial defence, and tails become aerodynamically disadvantageous if the wings provide sufficient lift. Derived hummingbird lineages also demonstrated the same expansion of tail shape and taxonomic diversity associated with perfection of the modern wing stroke mechanism earlier in avian history. Thus, living hummingbirds are a microcosm of overall avian flight evolution. Other living avian (‘aerial courser') and extinct reptilian (Pterosaur) clades with extraordinary flight abilities provide evidence for similar patterns, suggesting a broadly defined uniformitarianism (early constraint followed by later radiation) at the limits of the flight performance envelope throughout vertebrate history. Correlated evolution of TPB and tail form suggests that natural selection on an integrated flight system was the principal mechanism fostering the avian patterns, although strengthening of wing muscles in derived lineages may have facilitated expansion of caudal morphological diversity through a balance between natural and sexual selection on males. These findings suggest that wing muscles, locomotor integration, and phylogenetic patterns are essential for understanding function and adaptation of tails in living as well as ancient birds. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 467–493.