Flightless Research Articles

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.

Tarsometatarsus, eggshells, and the species level identification of large‐sized flightless birds from Boyo Paso 2 (Sierras of Córdoba, Argentina)

AbstractThe article presents the taxonomic study carried out on the Rheidae (Palaeognathae: Ratitae) faunal remains recovered in the open‐air archaeological site Boyo Paso 2 dated at approximately 1500–750 years BP (Sierras of Córdoba, Argentina). The study is focused on an adult proximal tarsometatarsus, a juvenile distal tarsometatarsus and 453 eggshell remains. The specimens were identified to its most specific level exploring and describing the diagnostic keys to species/genera level identification in modern reference collections. Two Rheidae species were identified: Rhea cf. R. americana and Rhea cf. R. pennata. However, most specimens were assigned to Rhea sp., including the tarsometatarsus remains. Taxonomic assignments indicate that even with the adoption of plant cultivation approximately 1.500 years BP, a broad spectrum foraging base played a key role for late prehispanic daily subsistence, increasing now the number of identified species added to the subsistence as the one not previously considered R. pennata. Its identification also suggests that the late prehispanic environment presented a higher biodiversity than at present, being the modern landscape a nonaccurate analogue of past conditions. It is concluded that achieving taxonomic identification to the most specific possible level becomes the fundamental pillars to assess the taxonomic diversity of human past subsistence as well as characterize the paleoenvironment, which mixed cultivation and foraging people interacted.

Repeated evolution of flightlessness in Dryolimnas rails (Aves: Rallidae) after extinction and recolonization on Aldabra

AbstractThe Aldabra rail, Dryolimnas cuvieri subsp. aldabranus, endemic to the Aldabra Atoll, Seychelles, is the last surviving flightless bird in the Indian Ocean. Aldabra has undergone at least one major, total inundation event during an Upper Pleistocene (Tarantian age) sea-level high-stand, resulting in the loss of all terrestrial fauna. A flightless Dryolimnas has been identified from two temporally separated Aldabran fossil localities, deposited before and after the inundation event, providing irrefutable evidence that a member of Rallidae colonized the atoll, most likely from Madagascar, and became flightless independently on each occasion. Fossil evidence presented here is unique for Rallidae and epitomizes the ability of birds from this clade to successfully colonize isolated islands and evolve flightlessness on multiple occasions.

Convergent regulatory evolution and loss of flight in paleognathous birds.

A core question in evolutionary biology is whether convergent phenotypic evolution is driven by convergent molecular changes in proteins or regulatory regions. We combined phylogenomic, developmental, and epigenomic analysis of 11 new genomes of paleognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight. A Bayesian analysis of 284,001 conserved noncoding elements, 60,665 of which are corroborated as enhancers by open chromatin states during development, identified 2355 independent accelerations along lineages of flightless paleognaths, with functional consequences for driving gene expression in the developing forelimb. Our results suggest that the genomic landscape associated with morphological convergence in ratites has a substantial shared regulatory component.

Turing patterning with and without a global wave.

Periodic patterning represents a fundamental process in tissue morphogenesis. In chicken dorsal skin, feather formation starts from the midline; then the morphogenetic wave propagates bilaterally, leaving a regular hexagonal array of feather germs. Yet, in vitro reconstitution showed feather germs appear simultaneously, leading to the hypothesis that the feather-forming wave results from the coupling of local Turing patterning processes with an unidentified global event. In this issue, Ho and colleagues showed such a global event in chicken feathers involves a spreading Ectodysplasin A (EDA) wave and Fibroblast Growth Factor 20 (FGF20)-cell aggregate-based mechanochemical coupling. In flightless birds, feather germs form periodically but without precise hexagonal patterning due to the lack of global wave.

Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees

Conservation of DNA sequence over evolutionary time is a strong indicator of function, and gain or loss of sequence conservation can be used to infer changes in function across a phylogeny. Changes in evolutionary rates on particular lineages in a phylogeny can indicate shared functional shifts, and thus can be used to detect genomic correlates of phenotypic convergence. However, existing methods do not allow easy detection of patterns of rate variation, which causes challenges for detecting convergent rate shifts or other complex evolutionary scenarios. Here we introduce PhyloAcc, a new Bayesian method to model substitution rate changes in conserved elements across a phylogeny. The method assumes several categories of substitution rate for each branch on the phylogenetic tree, estimates substitution rates per category, and detects changes of substitution rate as the posterior probability of a category switch. Simulations show that PhyloAcc can detect genomic regions with rate shifts in multiple target species better than previous methods and has a higher accuracy of reconstructing complex patterns of substitution rate changes than prevalent Bayesian relaxed clock models. We demonstrate the utility of PhyloAcc in two classic examples of convergent phenotypes: loss of flight in birds and the transition to marine life in mammals. In each case, our approach reveals numerous examples of conserved nonexonic elements with accelerations specific to the phenotypically convergent lineages. Our method is widely applicable to any set of conserved elements where multiple rate changes are expected on a phylogeny.

Mitochondrial Genomes from New Zealand’s Extinct Adzebills (Aves: Aptornithidae: Aptornis) Support a Sister-Taxon Relationship with the Afro-Madagascan Sarothruridae

The recently extinct New Zealand adzebills (Aptornithidae, Aptornis spp.) were an enigmatic group of large flightless birds that have long eluded precise taxonomic assignment as they do not closely resemble any extant birds. Adzebills were nearly wingless, weighed approximately 16–19 kg, and possessed massive adze-like reinforced bills whose function remains unknown. Using hybridisation enrichment and high-throughput sequencing of DNA extracted from subfossil bone and eggshell, near-complete mitochondrial genomes were successfully assembled from the two Quaternary adzebill species: the North Island Adzebill (Aptornis otidiformis) and South Island Adzebill (A. defossor). Molecular phylogenetic analyses confirm that adzebills are members of the Ralloidea (rails and allies) and are sister-taxon to the Sarothruridae, which our results suggest comprises the Madagascan wood rails (Mentocrex, two likely sp.) in addition to the tiny (<50 gram) rail-like Afro-Madagascan flufftails (Sarothrura, 9 spp.). Node age estimates indicate that the split between adzebills and Sarothruridae occurred ~39.6 Ma, suggesting that the ancestors of the adzebills arrived in New Zealand by long-distance dispersal rather than continental vicariance. This newly identified biogeographic link between physically distant New Zealand and Afro-Madagascar, echoed by the relationship between the New Zealand kiwi (Apterygiformes) and Madagascan elephant-birds (Aepyornithiformes), suggests that the adzebill’s near relatives were formerly more widespread. In addition, our estimate for the divergence time between the two Quaternary adzebill species (0.2–2.3 Ma) coincides with the emergence of a land-bridge between the North and South islands of New Zealand (ca. 1.5–2 Ma). This relatively recent divergence suggests that North Island adzebills are the result of a relatively recent dispersal from the South Island, from which the earliest (Miocene) adzebill fossil has been described.

Comparison of the volume fraction values of grey matter on the cervical enlargement of the spinal cord in chicken and quail

The aim of this study was to estimate and compare volume fraction values of grey matter (substantia grisea) in the cervical enlargement (intumescentia cervicalis) using stereological methods for two different types of birds. Ten pairs of quails and chickens were included in this study as one of them is flying and the other one is flightless bird species. The tissues cut into serial sections of 5 µm thickness were selected according to systematic random sampling and stained with cresyl violet. Volume and volume fractions were calculated in accordance with the Cavalieri principle. Student’s t-test was used to evaluate volume fraction differences among the species. The volume fractions of grey matter in cervical enlargement of chicken and quail were 0.277 ± 0.005 and 0.346 ± 0.014 (Mean ± Standart Deviation), respectively (p < 0.001). There was a significant difference between chicken and quail cervical enlargements in terms of volume fraction values of grey matter. On the other hand, the Cavalieri principle was considered as an unbiased, accurate and effective method for volume and volume fraction estimations.

Insect wing loss is tightly linked to the treeline: evidence from a diverse stonefly assemblage

The secondary loss of flight in previously winged insect lineages has long fascinated biologists. Habitat stability and isolation are thought to play important roles in driving wing reduction (Roff 1990, 1994), with exposure to high winds suggested to accelerate this process (Darwin 1859), although the role exposure plays in insect wing loss has never been empirically demonstrated. Here we assess fine‐scale distributional records from a diverse regional stonefly assemblage, to demonstrate a widespread association between wing loss and the treeline in New Zealand. The observed pattern suggests that exposure plays a crucial role driving wing loss in alpine insects.

Flightless birds are not neuroanatomical analogs of non-avian dinosaurs

BackgroundIn 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).ResultsWhile 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.ConclusionThe 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.

The origin of the world’s smallest flightless bird, the Inaccessible Island Rail Atlantisia rogersi (Aves: Rallidae)

Rails (Aves: Rallidae) are renowned for their extreme dispersal capability, which has given rise to numerous island lineages. Many insular species lost the ability to fly as a response to release from predator pressure—a feature causing rapid extinction when humans subsequently introduced mammals. The world’s smallest extant flightless bird, the Inaccessible Island Rail Atlantisia rogersi, is endemic to Inaccessible Island, Tristan da Cunha archipelago, in the central South Atlantic Ocean. It is placed in a monotypic genus, but its taxonomic affinity, as well as geographic origin, are disputed. Contrary to its suggested Old World origin, we demonstrate that the Inaccessible Island Rail is nested within the mainly South American ‘Laterallus clade’ and that it colonized ≥3 million-year-old Inaccessible Island from South America c. 1.5 million years ago. The taxonomy of rails has traditionally been based on morphology, and convergent evolution has caused many cases of misclassification. We suggest a re-classification within the ‘Laterallus clade’ and call for extended coverage of taxon sampling for DNA sequencing.

Novel genetic variation in an isolated population of the nationally critical Haast tokoeka (Apteryx australis ‘Haast’) reveals extreme short-range structure within this cryptic and flightless bird

There are currently five recognised species of kiwi (Apteryx spp.), and possibly 11 distinct genetic lineages, all of which are threatened or near threatened. Currently, with only approximately 400 individuals left, the most endangered provenance is Haast tokoeka (Apteryx australis ‘Haast’), classified as ‘Nationally Critical’ (Robertson et al. 2017 in Conservation status of New Zealand birds, 2016. New Zealand Threat Classification Series 19. Department of Conservation, Wellington). Several decades ago, a population of tokoeka from the Upper Arawhata region of the Olivine ranges near Haast, New Zealand was discovered, separated from the Lower Arawhata population by the Arawhata River and up to 20 km distance. Here, we used 1283 basepairs from two mitochondrial loci (control region and cytochrome b) and 14 nuclear microsatellites to describe the genetic diversity of this discrete population. Compared to Lower Arawhata, mitochondrial diversity was greater in Upper Arawhata with three mtDNA haplotypes compared to two, despite a lower sample size, and a pairwise nucleotide diversity more than five times as high (π = 0.00082). No mtDNA haplotypes were shared between the two regions. Microsatellites revealed moderate inbreeding in Upper Arawhata (FIS = 0.102), lower diversity levels to Lower Arawhata, and indicated this population is closest to but distinct from Lower Arawhata tokoeka when compared to other recognised tokoeka provenances. The marker-specific disparity in diversity measurements in Upper Arawhata may reflect relatedness in the presence of female dispersal. The low mitochondrial diversity in Lower Arawhata may indicate an over-use of productive females in supplementation programs. The distribution of genetic variation across all tokoeka was consistent with an isolation-by-distance model, but this correlation may be disrupted by local and complete barriers to gene flow creating highly structured regional populations. In summary, we provide strong support for the classification of the Upper Arawhata tokoeka as a genetically distinct population, increasing the genetic variation within Haast tokoeka and providing a useful resource for on-going conservation management.

Review of the vertebrate-mediated dispersal of the Date Palm, Phoenix dactylifera

As a major agricultural crop in the semi-arid and arid zone of North Africa and the Middle East, drupes (“fruits”) of the Date Palm Phoenix dactylifera form with their high carbohydrate content of the flesh and oils in the seed a major part of the diet of resident and migratory bird species and fruit bats. This paper reviews the range of known instances of drupe predation by volant and non-volant vertebrate vectors. While documented dispersal distances range from tens of metres to about 50 km, the efficacy of that dispersal has not been assessed in any of the papers under review. While volant animals, primarily birds, make up the greatest number of dispersal vectors and also account for the greatest number of seeds dispersed, long distance dispersal of a larger quantity of seeds per dispersal event seems to rely on terrestrial animals, primarily canids, but also bears and flightless birds, such as the Emu (Dromaius novaehollandiae).

FMRFa receptor stimulated Ca2+ signals alter the activity of flight modulating central dopaminergic neurons in Drosophila melanogaster.

Neuropeptide signaling influences animal behavior by modulating neuronal activity and thus altering circuit dynamics. Insect flight is a key innate behavior that very likely requires robust neuromodulation. Cellular and molecular components that help modulate flight behavior are therefore of interest and require investigation. In a genetic RNAi screen for G-protein coupled receptors that regulate flight bout durations, we earlier identified several receptors, including the receptor for the neuropeptide FMRFa (FMRFaR). To further investigate modulation of insect flight by FMRFa we generated CRISPR-Cas9 mutants in the gene encoding the Drosophila FMRFaR. The mutants exhibit significant flight deficits with a focus in dopaminergic cells. Expression of a receptor specific RNAi in adult central dopaminergic neurons resulted in progressive loss of sustained flight. Further, genetic and cellular assays demonstrated that FMRFaR stimulates intracellular calcium signaling through the IP3R and helps maintain neuronal excitability in a subset of dopaminergic neurons for positive modulation of flight bout durations.

High sequence variation in the exon 10 of TSHR gene is associated with flightless-domestic geese.

The genetic and molecular mechanisms of the flightless birds without limb modification are rarely reported. To explore the possible reasons for losing flight ability without limb modification, we used the domestic geese as an ideal model to preliminarily study the possible mechanisms for this kind of flightlessness. We compared the sequence variations of the exon 10 of TSHR gene between three domesticated geese populations and two wild ancestor populations. The results showed that domestic geese had higher genetic diversity and more complex population structure than their wild ancestors. We did not detect any population expansion in domestic geese population. However, we detected clear relaxed selection signal and positive selection in domesticated geese groups. Furthermore, special phylogenetic relationship of the exon 10 of TSHR was observed in domesticated geese groups. Combined with its well-established function on metabolic regulation and photoperiod control, we speculate that relaxed selection of TSHR might have effects on flightlessness of domesticated geese.

Effect of Antipredator Training on Spatial Behaviour of Male and Female Greater RheasRhea americanaReintroduced Into the Wild

The Greater Rhea Rhea americana is a South-American flightless bird whose populations have decreased due to poaching and fragmentation of suitable habitats, and there has been an urgent need to carry out management practices to prevent local or regional extinctions. Several studies revealed that reintroduction might be an appropriate action for increasing the viability of wild populations of this species. Nevertheless, although this is a popular and useful conservation strategy, the animals to be released should be prepared against risks like predation and dispersion that could influence the post-release success. We evaluated the effect of an antipredator training applied to captive-bred Greater Rheas before they were released into the wild, on their dispersal and home range size and overlap, supposing that the trained animals would avoid dispersing into places with predators and, consequently, they would reduce their home range. We also studied the habitat use by the released rheas. Eleven trained and nine control (untrained) animals were marked and monitored two to four times per day during the first week, and from 4 to 19 consecutive days per month during four months, throughout the breeding and post-breeding seasons. The antipredator training affected the home range in different ways according to sex. Trained females exhibited smaller home ranges (mean ± S.E.: 0.54 ± 0.58 km2) than the rest of the individuals (control females 5.8 ± 0.75 km2, control and trained males: 2.11 ± 0.65 km2 and 2.96 ± 0.65 km2, respectively), whereas their overlap was greater (63.83 ± 16.95%) than that of the untrained females (24.04 ± 21.88%). Males of both experimental groups showed similar distances travelled (3.21 ± 0.29 km), which were also greater than those of females (2.21 ± 0.32 km). The home ranges of males were not influenced by the training and they showed a high degree of overlapping (among control males 29.96 ± 18.95%, and among trained males: 35.81 ± 18.95%). Both groups similarly used crops and in lesser extent open areas and grassland. Only the trained females reduced their movements and wandering as a result of the previous conditioning. They moved to crop or open areas, avoiding tall vegetation such as that present in grasslands, which may make difficult to detect predators. On the other hand, in the males, the influence of the reproductive season and the complex mating system exhibited by this species prevailed over the possible effects of training. Our work shows new and useful data about the spatial behaviour and reintroduction for conservation of the Greater Rhea.

Multiple origin of flightlessness in Phaneropterinae bushcrickets and redefinition of the tribus Odonturini (Orthoptera: Tettigonioidea: Phaneropteridae)

The possession of wings and ability to fly are a unifying character of higher insects, but secondary loss of wings is widespread. Within the bushcrickets, the subfamily Phaneropterinae (Orthoptera: Tettigonioidea) comprises more than 2000 predominantly long-winged species in the tropics. However, the roughly 300 European representatives are mainly short-winged. The systematics of these radiations have been unclear, leading to their unreliable formal treatment, which has hindered analysis of the evolutionary patterns of flight loss. A molecular phylogeny is presented for 42 short-winged species and members of all European long-winged genera based on the combined data from three nuclear gene sequences (18S, H3, ITS2). We found four phylogenetic lineages: (i) the first included the short-wing species of the genus Odontura; (ii) a further branch is represented by the South-American short-winged Cohnia andeana; (iii) an assemblage of long-wing taxa with a deep branching pattern includes the members of the tribes Acrometopini, Ducetiini, Phaneropterini, and Tylopsidini; (iv) a large group contained all short-winged taxa of the tribe Barbitistini. Phaneropterinae flightlessness originated twice in the Western Palaearctic, with a number of mainly allo- and parapatrically distributed species of the Barbistini in Southeastern Europe, and the Middle East and a limited number of Odontura species in Northern Africa and Southwestern Europe. Both short-winged lineages are well separated, which makes it necessary to restrict the tribe Odonturini to the West-Palaearctic genus Odontura. Other flightless genera previously included in the Odonturini are placed as incertae sedis until their phylogenetic position can be established.

Paleobiology of Giant Flightless Birds. By Delphine Angst and Eric Buffetaut. London (United Kingdom): ISTE Press; Academic Press. Amsterdam (The Netherlands) and New York: Elsevier. $131.25. xiv + 281 p.; ill.; index. ISBN: 978-1-78548-136-9. 2017.

Previous articleNext article No AccessPaleontologyPaleobiology of Giant Flightless Birds. By Delphine Angst and Eric Buffetaut. London (United Kingdom): ISTE Press; Academic Press. Amsterdam (The Netherlands) and New York: Elsevier. $131.25. xiv + 281 p.; ill.; index. ISBN: 978-1-78548-136-9. 2017.John BoisJohn BoisScience, DeSoto County High School, Arcadia, Florida Search for more articles by this author Science, DeSoto County High School, Arcadia, FloridaPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The Quarterly Review of Biology Volume 93, Number 2June 2018 Published in association with Stony Brook University Article DOIhttps://doi.org/10.1086/698038 Views: 18Total views on this site For permission to reuse, please contact [email protected]PDF download Crossref reports no articles citing this article.

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus.

Understanding the mutualistic services provided by species is critical when considering both the consequences of their loss or the benefits of their reintroduction. Like many other Pacific islands, New Zealand seed dispersal networks have been changed by both significant losses of large frugivorous birds and the introduction of invasive mammals. These changes are particularly concerning when important dispersers remain unidentified. We tested the impact of frugivore declines and invasive seed predators on seed dispersal for an endemic tree, hinau Elaeocarpus dentatus, by comparing seed dispersal and predation rates on the mainland of New Zealand with offshore sanctuary islands with higher bird and lower mammal numbers. We used cameras and seed traps to measure predation and dispersal from the ground and canopy, respectively. We found that canopy fruit handling rates (an index of dispersal quantity) were poor even on island sanctuaries (only 14% of seeds captured below parent trees on islands had passed through a bird), which suggests that hinau may be adapted for ground‐based dispersal by flightless birds. Ground‐based dispersal of hinau was low on the New Zealand mainland compared to sanctuary islands (4% of seeds dispersed on the mainland vs. 76% dispersed on islands), due to low frugivore numbers. A flightless endemic rail (Gallirallus australis) conducted the majority of ground‐based fruit removal on islands. Despite being threatened, this rail is controversial in restoration projects because of its predatory impacts on native fauna. Our study demonstrates the importance of testing which species perform important mutualistic services, rather than simply relying on logical assumptions.

A mathematical model for pressure-based organs behaving as biological pressure vessels

We introduce a mathematical model that describes the allometry of physical characteristics of hollow organs behaving as pressure vessels based on the physics of ideal pressure vessels. The model was validated by studying parameters such as body and organ mass, systolic and diastolic pressures, internal and external dimensions, pressurization energy and organ energy output measurements of pressure-based organs in a wide range of mammals and birds. Seven rules were derived that govern amongst others, lack of size efficiency on scaling to larger organ sizes, matching organ size in the same species, equal relative efficiency in pressurization energy across species and direct size matching between organ mass and mass of contents. The lung, heart and bladder follow these predicted theoretical relationships with a similar relative efficiency across various mammalian and avian species; an exception is cardiac output in mammals with a mass exceeding 10 kg. This may limit massive body size in mammals, breaking Cope's rule that populations evolve to increase in body size over time. Such a limit was not found in large flightless birds exceeding 100 kg, leading to speculation about unlimited dinosaur size should dinosaurs carry avian-like cardiac characteristics.