The role of wing length in the evolution of avian flightlessness

Flightlessness has evolved independently in at least 11 extant avian families. A number of hypotheses have been proposed to explain these transitions in individual families, including release from predation on oceanic islands, energetic costs of flight and use of forelimbs for activities other than flying. Few studies have sought to explore factors common to all families containing flightless species, which may explain the taxonomic distribution of flightlessness. In this study, we found that for all eight avian families which contain both flightless and flighted species, the flighted species have shorter wing lengths relative to body mass than their sister families. This result is not biased by taxon size. Models of avian aerodynamics predict that birds with relatively short wings pay a high energetic cost of flight. We suggest that these increased energetic costs of flying predispose these avian families to evolve flightless species. The various causes for the shortening of wings among flighted species of birds and the possibility of future transitions to flightlessness are discussed.     

The evolution of flightlessness: Is history important?

Summary Though most birds and insects are capable of flight (volant) some species are flightless. In this paper I test the hypothesis that phylogenetic constraints have played a role in the evolution of flightlessness. If speciation occurred after the evolutionary transition to flightlessness, inferences concerning the importance of particular aspects of the environment on the probability of the evolution of flightlessness may be statistically spurious because of the inflation of the sample size. Among birds, ratites and penguins illustrate the phenomenon of considerable speciation subsequent to the transition to the evolution of flightlessness. In contrast, the rails represent a group in which each flightless species probably represents a separate evolutionary transition. There are many more flightless insect species than bird species and several orders are monomorphically flightless, the sometimes enormous speciation within the order following and possibly being a consequence of the evolution of flightlessness. While it can be shown in insects that flightlessness has evolved independently many times, there are at least as many cases in which the question cannot be resolved. Therefore, in both birds and insects phylogenetic effects should not be ignored, for the number of evolutionary transitions may be much less than the number of species. The effect of incorporating phylogenetic (or at least taxonomic) constraints into the analysis of habitat factors associated with flightlessness is considered.     

FLIGHTLESSNESS IN STEAMER-DUCKS (ANATIDAE: TACHYERES): ITS MORPHOLOGICAL BASES AND PROBABLE EVOLUTION

Flightlessness in Tachyeres is caused by wing-loadings in excess of 2.5 g·cm^–2, which result from the large body size and small wing areas of the flightless species. Reduced wing areas of flightless species are related to absolutely shorter remiges, and to relatively or absolutely shortened wing bones, although these reductions differ among species. Reduced lengths of the ulna, radius, and carpometacarpus are associated most strongly with flightlessness. Pectoral muscles and the associated sternal keel are well developed in all species of Tachyeres, largely because of the use of wings in “steaming,” an important locomotor behavior. Relative size of these muscles was greatest in largely flighted T. patachonicus; however, sexual dimorphism in wing-loadings results in flightlessness in some males of this species. Proportions in the wing skeleton, intraspecific allometry, and limited data on growth indicate that the relatively short wing bones and remiges of flightless Tachyeres are produced developmentally by a delay in the growth of wing components, and that this heterochrony may underlie, in part, skeletal sexual dimorphism. Increased body size in flightless steamer-ducks is advantageous in territorial defense of food resources and young, and perhaps diving in cold, turbulent water; reductions in wing area probably reflect refinements for wing-assisted locomotion and combat. Flightlessness in steamer-ducks is not related to relaxed predation pressure, but instead was permitted selectively by the year-round habitability of the southern South American coasts. These conditions not only permitted the success of the three flightless species of Tachyeres, but at present may be moving marine populations of T. patachonicus toward flightlessness.     

Flightlessness affects cranial morphology in birds

Flightless birds belonging to phylogenetically distant clades share several morphological features in the pectoral and pelvic apparatus. There are indications that skull morphology is also influenced by flightlessness. In this study we used a large number of flightless species to test whether flightlessness in modern birds does indeed affect cranial morphology. Discriminant analyses and variation partitioning show evidence for a relationship between skull morphology and the flightless condition in birds. A possible explanation for the change in cranial morphology can be linked to the reduced selective force for light-weight skulls in flightless birds. This makes an increase in muscle mass, and therefore an enlargement of muscle insertion areas on the skull, possible. We also compared the ontogenetic trajectory of Gallus with the adult morphology of a sample of flightless species to see whether the apomorphic features characterizing the skull of flightless birds share the same developmental basis, which would indicate convergent evolution by parallelism. Skull morphology (expressed as principal component scores) of palaeognathous flightless birds (ratites) is dissimilar (higher scores) to juvenile stages of the chicken and therefore seem peramorphic (overdeveloped). Principal component scores of adult neognathous flightless birds fall within the range of chicken development, so no clear conclusions about the ontogenetic trajectories leading to their sturdier skull morphology could be drawn.     

The primary feather lengths of early birds with respect to avian wing shape evolution

We examine the relationships between primary feather length (f(prim)) and total arm length (ta) (sum of humerus, ulna and manus lengths) in Mesozoic fossil birds to address one aspect of avian wing shape evolution. Analyses show that there are significant differences in the composition of the wing between the known lineages of basal birds and that mean f(prim) (relative to ta length) is significantly shorter in Archaeopteryx and enantiornithines than it is in Confuciusornithidae and in living birds. Based on outgroup comparisons with nonavian theropods that preserve forelimb primary feathers, we show that the possession of a relatively shorter f(prim) (relative to ta length) must be the primitive condition for Aves. There is also a clear phylogenetic trend in relative primary feather length throughout bird evolution: our analyses demonstrate that the f(prim)/ta ratio increases among successive lineages of Mesozoic birds towards the crown of the tree ('modern birds'; Neornithes). Variance in this ratio also coincides with the enormous evolutionary radiation at the base of Neornithes. Because the f(prim)/ta ratio is linked to flight mode and performance in living birds, further comparisons of wing proportions among Mesozoic avians will prove informative and certainly imply that the aerial locomotion of the Early Cretaceous Confuciusornis was very different to other extinct and living birds.     

Avian brachial index and wing kinematics: putting movement back into bones

The relationship between wing kinematics, wing morphology and the brachial index of birds (BI=humerus length/ulna length) was examined. BI was found to differ between three groups of birds, which were classified on the basis of similar wing kinematics. In addition, a comparative analysis of a large dataset, using phylogenetically independent contrasts, suggested a significant, albeit weak, correlation between BI and four measures of wing morphology (wing loading, wing area, wing length and aspect ratio). Although wing kinematics and wing morphology are both correlated with BI in birds, the dominant selective pressure upon this ratio is probably wing kinematics. The previously identified clade specificity of BI within Neornithes is most likely because birds with similar BIs fly with kinematic similarity and closely related birds have similar flight styles. A correlation between BI and wing kinematics means that it may be possible to characterize the wing beat of fossil birds. A more robust relationship between wing morphology and BI may emerge, but only after the relationship between wing kinematics and BI is quantified. A comparative and quantitative study of wing-bone anatomy and wing kinematics is a priority for future studies of avian wing-skeleton evolution and functional morphology.     

Relationships of the extinct moa-nalos, flightless Hawaiian waterfowl, based on ancient DNA

The extinct moa-nalos were very large, flightless waterfowl from the Hawaiian islands. We extracted, amplified and sequenced mitochondrial DNA from fossil moa-nalo bones to determine their systematic relationships and lend insight into their biogeographical history. The closest living relatives of these massive, goose-like birds are the familiar dabbling ducks (tribe Anatini). Moa-nalos, however, are not closely related to any one extant species, but represent an ancient lineage that colonized the Hawaiian islands and evolved flightlessness long before the emergence of the youngest island, Hawaii, from which they are absent. Ancient DNA yields a novel hypothesis for the relationships of these bizarre birds, whereas the evidence of phylogeny in morphological characters was obscured by the evolutionary transformation of a small, volant duck into a giant, terrestrial herbivore.     

Wing-bone length allometry in birds

A comparative analysis using both independent contrasts (CAIC) and a species level analysis was used to investigate the allometric scaling of avian wing-bone lengths. Total arm ( ta =humerus+ulna+manus) scaled with positive allometry as body mass ( M )^0.37–0.39. Similarly, and in accordance with previous studies, wing-span ( b ) was positively allometric, but CAIC suggested a lower allometric exponent ( M ^0.35) than found using species as independent data points ( M ^0.39). Contrary to previous studies, individual wing-bones appear to scale with similar exponents against M and scale isometrically with ta . In addition to a general trend for larger birds to have longer wings, wing-bones and ta , their ta was a larger proportion of their b . A detailed study of primary feather length and elbow joint angle across a wide range of bird species and bird size, however, is required before a conclusive explanation for this increase in ta relative to b in larger birds can be established. Scaling equations are presented that can be used to predict M , ta and b from individual wing-bone lengths, which may be of use to palaeontologists wishing to reconstruct whole animals from single bones.     

Genetic tests of rapid parallel speciation of flightless birds from an extant volant ancestor

Prior to the extinction wave that followed the human colonization of Oceania, flightless rails (Aves: Rallidae) were among the largest radiations of island birds, and perhaps the most species-rich example of convergent evolution in vertebrates. Insular flightless species are thought to have evolved from extant, volant species that colonized from continental sources and rapidly followed parallel adaptive pathways to flightlessness. The present study provides the first test of this model of speciation using genetic data sampled throughout the range of a putative ancestral species. Mitochondrial control region sequences from 71 individuals of the Gallirallus philippensis species complex reveal essentially no geographic structure within archipelagos and only weak structure among archipelagos, with no major genetic breaks except for birds sampled in the Philippines. Demographic tests of coalescent models support a recent rapid expansion into Oceania (including Australia) out of the Philippines approximately 20 000 years ago. The estimated coalescence of G. philippensis mitochondrial alleles approximately 33 000 years ago closely corresponds to the expansion of humans into the archipelagoes of Near Oceania, suggesting that humans may have facilitated its colonization by exterminating flightless competitors and clearing lowland forests. Phylogenetic analyses that included all G. philippensis haplotypes and samples from 11 single-island endemic flightless species of Gallirallus indicate that G. philippensis is polyphyletic, but is not the ancestor of most of its flightless congeners, as previously thought. Nuclear gene sequences (β-actin inron 3) suggest that G. philippensis polyphyly is at least partly due to hybridization. The flightless condition evolves in rails before reproductive isolation is complete.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 601–616.     

Morphological and histological examination of short‐wing formation in the winter moth Protalcis concinnata (Insecta: Lepidoptera,Geometridae)

Winter geometrid moths exhibit sexual dimorphism in wing length and female‐specific flightlessness. Female‐specific flightlessness in insects is an interesting phenomenon in terms of sexual dimorphism and reproductive biology. In the winter geometrid moth, Protalcis concinnata (Wileman), adult females have short wings and adult males have fully developed wings. Although the developmental process for wing reduction in Lepidoptera is well studied, little is known about the morphology and the developmental pattern of short‐winged flightless morphs in Lepidoptera. To clarify the precise mechanisms and developmental processes that produce short‐winged morphs, we performed morphological and histological investigations of adult and pupal wing development in the winter geometrid moth P. concinnata. Our findings showed that (a) wing development in both sexes is similar until larval‐pupal metamorphosis, (b) the shape of the sexually dimorphic wings is determined by the position of the bordering lacuna (BL), (c) the BL is positioned farther inward in females than in males, and (d) after the short pupal diapause period, the female pupal wing epithelium degenerates to approximately two‐thirds its original size due to cell death. We propose that this developmental pattern is a previously unrecognized process among flightless Lepidoptera.     

FLIGHTLESSNESS IN GREBES (AVES,PODICIPEDIDAE): ITS INDEPENDENT EVOLUTION IN THREE GENERA

The morphological bases of flightlessness in three genera of grebes were studied using 790 study skins, 322 skeletons, myological data from 40 anatomical specimens studied by Sanders (1967), and ancillary data on wing-loadings. Three species, Rollandia microptera, Podilymbus gigas, and Podiceps taczanowskii, are considered to be flightless; each is endemic to a high-altitude, neotropical lake or lake system. Compared to their flighted (capable of flight) sister-species, the three flightless species shared several broadly convergent characters: larger body mass and skeletal dimensions (exclusive of the sternal carina), reductions in relative lengths of wing, tail, and primary remiges, and reduction in the relative size of breast muscles. Rollandia microptera exhibited the greatest morphological differences from its flighted sister-species; these differences were comparable to intergeneric morphometric differences in magnitude and involved a tripling of body mass, a modal loss of one primary remex in each wing, absolute reduction of the sternal carina, flattening of proximal wing elements, a large morphometric shift in skeletal dimensions, an increase in the scapulocoracoid angle, and six qualitative differences in the pectoral musculature. Morphological differences between Podilymbus gigas and its flighted congener were comparatively minor; flightlessness in this species, if genuine, evidently results from an allometric increase in size combined with a large decrease in relative bulk of breast musculature and shift of alar muscle mass. Podiceps taczanowskii was intermediate in degree of anatomical difference from its flighted relatives, but was unique in its slight reduction in absolute length of the wings and decrease in absolute widths of the skeletal wing elements. Multivariate differences in external characters associated with flightlessness were strongly convergent in the three genera, but multivariate differences in skeletal proportions differed substantially among genera in detail. An estimate of wing-loading indicated that Podilymbus gigas and, especially, Podiceps taczanowskii may be only “flight-impaired” rather than flightless. Relative wing lengths and conformation of sterna in Rollandia microptera and Podiceps taczanowskii indicate that morphological changes associated with flightlessness are paedomorphic; intraspecific allometry in Rollandia indicates that the underlying ontogenetic change may involve a delay in the start of pectoral-alar development (postdisplacement). Flightlessness in grebes, a family typified by moderately heavy wing-loadings and relatively small pectoral muscles, is related in all three instances to the year-round residency afforded by large lakes at low latitudes. The primary selective advantages of morphological changes leading to flightlessness probably are related to the thermodynamic advantages of increased body sizes, feeding specialization associated with enlargement of the bill, and reduction of intraspecific niche overlap through increased sexual dimorphism; the changes are also possibly related to economy of pectoral-alar development.     

Immunohistochemical study of cutaneous nerves in the emu

The distribution and chemical content of cutaneous nerves in 3- to 13-day-old emu chicks (Dromaius novaehollandiae) were examined by using double-labelling immunohistochemistry. Seven different subpopulations of cutaneous nerves were identified based on their neurochemistry. No intraepidermal nerve fibres were found. However, axons were located within the dermis and were often associated with blood vessels, pennamotor muscles and feather follicles or innervated Herbst corpuscles. Both similarities and differences exist between subpopulations of cutaneous nerves in the emu and volant birds. As in volant birds, a subpopulation of cutaneous axons innervates the superficial skin layers and contains immunoreactivity to both substance P and calcitonin gene-related peptide (CGRP). This suggests that the neuropeptide content of these presumptive free nerve endings is conserved throughout the evolution of birds. In contrast, Herbst corpuscles in the emu are innervated by axons that contain immunoreactivity for CGRP or neuropeptide Y (NPY) but that lack the calbindin D-28k immunoreactivity found in fibres innervating Herbst corpuscles of volant birds. Herbst corpuscles therefore may have a different chemical content in a flightless species from that in volant birds.This work was supported by an Australian Postgraduate Award (Industry; CO9942100) and the Flinders Institute for Health and Medical Research.     

Gradual evolution towards flightlessness in steamer ducks*

Flightlessness in birds is the product of changes in suites of characters—including increased body size and reduced anterior limbs—that have evolved repeatedly and independently under similar ecological conditions (generally insularity). It remains unknown whether this phenotypic convergence extends to the genomic level, partially because many losses of flight occurred long ago (such as in penguins or ratites), thus complicating the study of the genetic pathways to flightlessness. Here, we use genome sequencing to study the evolution of flightlessness in a group of ducks that are current and dynamic exemplars of this major functional transition. These recently diverged Tachyeres steamer ducks differ in their ability to fly: one species is predominantly flighted and three are mainly flightless. Through a genome‐wide association analysis, we identify two narrow candidate genomic regions implicated in the morphological changes that led to flightlessness, and reconstruct the number of times flightlessness has evolved in Tachyeres. The strongest association is with DYRK1A, a gene that when knocked out in mice leads to alterations in growth and bone morphogenesis. These findings, together with phylogenetic and demographic analyses, imply that the genomic changes leading to flightlessness in Tachyeres may have evolved once, and that this trait remains functionally polymorphic in two species.     

Ecological factors affect the level and scaling of avian BMR

The basal rate of metabolism (BMR) in 533 species of birds, when examined with ANCOVA, principally correlates with body mass, most of the residual variation correlating with food habits, climate, habitat, a volant or flightless condition, use or not of torpor, and a highland or lowland distribution. Avian BMR also correlates with migratory habits, if climate and a montane distribution is excluded from the analysis, and with an occurrence on small islands if a flightless condition and migration are excluded. Residual variation correlates with membership in avian orders and families principally because these groups are behaviorally and ecologically distinctive. However, the distinction between passerines and other birds remains a significant correlate of avian BMR, even after six ecological factors are included, with other birds having BMRs that averaged 74% of the passerine mean. This combination of factors accounts for 97.7% of the variation in avian BMR. Yet, migratory species that belong to Anseriformes, Charadriiformes, Pelecaniformes, and Procellariiformes and breed in temperate or polar environments have mass-independent basal rates equal to those found in passerines. In contrast, penguins belong to an order of polar, aquatic birds that have basal rates lower than passerines because their flightless condition depresses basal rate. Passerines dominate temperate, terrestrial environments and the four orders of aquatic birds dominate temperate and polar aquatic environments because their high BMRs facilitate reproduction and migration. The low BMRs of tropical passerines may reflect a sedentary lifestyle as much as a life in a tropical climate. Birds have BMRs that are 30-40% greater than mammals because of the commitment of birds to an expensive and expansive form of flight.     

A new brachypterous Nusalala species from Costa Rica, with comments on the evolution of flightlessness in brown lacewings (Neuroptera: Hemerobiidae)

Abstract. A new flightless hemerobiid species, Nusalala brachyptera , collected at high elevation in Costa Rica, is described and illustrated, and a variety of data relevant to the evolution of flightlessness in the family Hemerobiidae are reviewed. Flightlessness due to brachyptery has evolved independently in at least five monophyletic [= holophyletic] lineages of the family Hemerobiidae (brown lacewings). Volant hemerobiids are primarily foliage foraging arboreal predators [presumed ancestral condition], while flightless species are predominantly associated with terricolous-type microhabitats (e.g. ground-litter, epiphytic mosses) [presumed derived condition]. These differences suggest a significant habitat shift for flightless hemerobiid species, and that the parallel evolution of flightlessness and brachyptery in hemerobiids are shared responses to the conditions of a terricolous existence. The restriction of most flightless hemerobiid species to insular and/or montane/alpine land areas may be related to the typically depauperate nature of the faunas of such areas. This faunal characteristic may facilitate transitions from arboreality to terricolousness by presenting ancestrally arboreal predators such as hemerobiids with novel ecological opportunities in terricolous microhabitats.     

Greater energy stores enable flightless moulting geese to increase resting behaviour

Many species of waterfowl undergo a post‐breeding simultaneous flight feather moult (wing moult) which renders them flightless and vulnerable to predation for up to 4 weeks. Here we present an analysis of the correlations between individual time‐budgets and body mass states in 13 captive Barnacle Geese Branta leucopsis throughout an entire wing moult. The daily percentage of time spent resting was positively correlated with initial body mass at the start of wing moult. Behaviour of individual birds during wing moult is dependent on initial physiological state, which may in turn be dependent on foraging ability; the storage of energy before the start of wing moult will help birds to reduce exposure to the dangers of predation.     

Panbiogeography and rails of the genus Gallirallus

Abstract

An investigation of flightlessness in the Rallidae led me to question the theories of Olson (1973); that all rails in the genus Gallirallus were distributed over their present range by recent flighted dispersal; and that flightlessness is a recent process conferred by the paedomorphic process neoteny. The current distribution of some members of Gallirallus (Olson 1973a) are interpreted using the panbiogeographic method of Croizat (1958, 1958a). This method indicates that the distribution of some rails is similar to other biota. I suggest the group may be ancient, and its distribution the result of vicariism. Consequently, the evolution of flightless morphology need not be fast, and the flightless rails on different land masses could be the result of flightless radiations.     

Flightless birds are not neuroanatomical analogs of non-avian dinosaurs

Background

In comparative neurobiology, major transitions in behavior are thought to be associated with proportional size changes in brain regions. Bird-line theropod dinosaurs underwent a drastic locomotory shift from terrestrial to volant forms, accompanied by a suite of well-documented postcranial adaptations. To elucidate the potential impact of this locomotor shift on neuroanatomy, we first tested for a correlation between loss of flight in extant birds and whether the brain morphology of these birds resembles that of their flightless, non-avian dinosaurian ancestors. We constructed virtual endocasts of the braincase for 80 individuals of non-avian and avian theropods, including 25 flying and 19 flightless species of crown group birds. The endocasts were analyzed using a three-dimensional (3-D) geometric morphometric approach to assess changes in brain shape along the dinosaur-bird transition and secondary losses of flight in crown-group birds (Aves).

Results

While non-avian dinosaurs and crown-group birds are clearly distinct in endocranial shape, volant and flightless birds overlap considerably in brain morphology. Phylogenetically informed analyses show that locomotory mode does not significantly account for neuroanatomical variation in crown-group birds. Linear discriminant analysis (LDA) also indicates poor predictive power of neuroanatomical shape for inferring locomotory mode. Given current sampling, Archaeopteryx, typically considered the oldest known bird, is inferred to be terrestrial based on its endocranial morphology.

Conclusion

The results demonstrate that loss of flight does not correlate with an appreciable amount of neuroanatomical changes across Aves, but rather is partially constrained due to phylogenetic inertia, evident from sister taxa having similarly shaped endocasts. Although the present study does not explicitly test whether endocranial changes along the dinosaur-bird transition are due to the acquisition of powered flight, the prominent relative expansion of the cerebrum, in areas associated with flight-related cognitive capacity, suggests that the acquisition of flight may have been an important initial driver of brain shape evolution in theropods.

     

Metabolic ‘engines’ of flight drive genome size reduction in birds

The tendency for flying organisms to possess small genomes has been interpreted as evidence of natural selection acting on the physical size of the genome. Nonetheless, the flight–genome link and its mechanistic basis have yet to be well established by comparative studies within a volant clade. Is there a particular functional aspect of flight such as brisk metabolism, lift production or maneuverability that impinges on the physical genome? We measured genome sizes, wing dimensions and heart, flight muscle and body masses from a phylogenetically diverse set of bird species. In phylogenetically controlled analyses, we found that genome size was negatively correlated with relative flight muscle size and heart index (i.e. ratio of heart to body mass), but positively correlated with body mass and wing loading. The proportional masses of the flight muscles and heart were the most important parameters explaining variation in genome size in multivariate models. Hence, the metabolic intensity of powered flight appears to have driven genome size reduction in birds.     

Wing shape and migration in shorebirds: a comparative study

Migration is an energetically expensive and hazardous stage of the annual cycle of non‐resident avian species, and requires certain morphological adaptations. Wing shape is one of the morphological traits that is expected to be evolutionarily shaped by migration. Aerodynamic theory predicts that long‐distance migrants should have more pointed wings with distal primaries relatively longer than proximal primaries, an arrangement that minimizes induced drag and wing inertia, but this prediction has mostly been tested in passerine species. We applied the comparative method of phylogenetically independent contrasts to assess convergent evolution between wing shape and migration within shorebirds. We confirmed the assumption that long‐distance migrants have less rounded wings than species migrating shorter distances. Furthermore, wing roundedness negatively correlates with fat load and mean distance of migratory flights, the basic components of migration strategies. After controlling for interspecific differences in body size, we found no support for a link between wing length and migration, indicating that wing shape is a more important predictor of shorebird migratory behaviour than wing length. The results suggest that total migration distance and migratory strategy may simultaneously act on the evolution of wing shape in shorebirds, and possibly in other avian species.