Predictable evolution toward flightlessness in volant island birds

Abstract

Birds are prolific colonists of islands, where they readily evolve distinct forms. Identifying predictable, directional patterns of evolutionary change in island birds, however, has proved challenging. The "island rule" predicts that island species evolve toward intermediate sizes, but its general applicability to birds is questionable. However, convergent evolution has clearly occurred in the island bird lineages that have undergone transitions to secondary flightlessness, a process involving drastic reduction of the flight muscles and enlargement of the hindlimbs. Here, we investigated whether volant island bird populations tend to change shape in a way that converges subtly on the flightless form. We found that island bird species have evolved smaller flight muscles than their continental relatives. Furthermore, in 366 populations of Caribbean and Pacific birds, smaller flight muscles and longer legs evolved in response to increasing insularity and, strikingly, the scarcity of avian and mammalian predators. On smaller islands with fewer predators, birds exhibited shifts in investment from forelimbs to hindlimbs that were qualitatively similar to anatomical rearrangements observed in flightless birds. These findings suggest that island bird populations tend to evolve on a trajectory toward flightlessness, even if most remain volant. This pattern was consistent across nine families and four orders that vary in lifestyle, foraging behavior, flight style, and body size. These predictable shifts in avian morphology may reduce the physical capacity for escape via flight and diminish the potential for small-island taxa to diversify via dispersal.B irds on islands helped to inspire the theory of evolution by natural selection (1, 2), and they continue to illuminate its mechanisms (e.g., ref.3). Some studies have reported that the bodies and bills of island birds systematically shift in size, reflecting evolution toward a generalist niche in species-poor communities (4-8). The tendency for island taxa to converge toward intermediate body size after colonizing islands is known as the island rule (4), but this ecogeographic rule has proven to be an inconsistent predictor of evolutionary trends in island bird populations (9-12). Detailed studies of island radiations have revealed idiosyncratic patterns of body size and bill size evolution among species, with morphological changes attributable to taxon-specific changes in foraging ecology (e.g., ref. 12). This inconsistency raises the question as to whether there are predictable evolutionary trends that apply generally to island birds.The most striking evolutionary trend among island birds is the loss of flight. Transitions to flightlessness are rapid and irreversible (13,14), with each instance involving the substantial reallocation of mass from the forelimbs to the hindlimbs and near elimination of costly flight muscles (15-18). More than 1,000 independent lineages of island birds have lost flight, including rails, parrots, pigeons, owls, waterfowl, and passerines (13-1...

How do seemingly non-vagile clades accomplish trans-marine dispersal? Trait and dispersal evolution in the landfowl (Aves: Galliformes)

“…Previous studies have reported increased body size [55], as well as rapid losses of dispersal ability [1], in lineages colonizing oceanic islands. Our results extend these findings to galliforms, and suggest that evidence for rare marine dispersal events by non-vagile taxa should be treated with caution, even when apparent cases derive from largely non-vagile clades.…”

“…Yet, paradoxically, organisms that lack dispersal capability are still characteristic components of isolated continents and island communities [1][2][3][4]. For example, large-bodied and flightless ratite birds (e.g.…”

A genetic signature of the evolution of loss of flight in the Galapagos cormorant

“…Moreover, recent studies strongly suggest that the ratites (ostriches, emus, rheas, cassowaries and kiwis), long thought to derive from a single flightless ancestor, may constitute a polyphyletic group characterized by multiple independent instances of loss of flight and convergent evolution (3–5). However, despite the ubiquity and evolutionary importance of loss of flight (6), the underlying genetic and molecular mechanisms remain unknown.…”

Origin, paleoecology, and extirpation of bluebirds and crossbills in the Bahamas across the last glacial–interglacial transition

“…Nevertheless, the Bahamian bluebird fossils do differ from all other forms of S. sialis in having a relatively short distal wing (low ratio of carpometacarpus length to humerus length; an exception being the single specimen of S. s. guatemalae from Chiapas) and a relatively large body for its wing size (high ratio of femur length to humerus length (32), although these ratios are not necessarily based on bones from the same individuals. These trends in the limb proportions of Bahamian Eastern bluebirds, which are to be expected in resident insular versus continental populations of conspecific volant songbirds (32,33), were not evident in the two bluebird skeletons from Bermuda (SI Appendix, Table S1). …”