Endocranial anatomy of the charadriiformes: sensory system variation and the evolution of wing-propelled diving.
ABSTRACT: Just as skeletal characteristics provide clues regarding behavior of extinct vertebrates, phylogenetically-informed evaluation of endocranial morphology facilitates comparisons among extinct taxa and extant taxa with known behavioral characteristics. Previous research has established that endocranial morphology varies across Aves; however, variation of those systems among closely related species remains largely unexplored. The Charadriiformes (shorebirds and allies) are an ecologically diverse clade with a comparatively rich fossil record, and therefore, are well suited for investigating interspecies variation, and potential links between endocranial morphology, phylogeny, ecology and other life history attributes. Endocranial endocasts were rendered from high resolution X-ray computed tomography data for 17 charadriiforms (15 extant and two flightless extinct species). Evaluation of endocranial character state changes on a phylogeny for Charadriiformes resulted in identification of characters that vary in taxa with distinct feeding and locomotor ecologies. In comparison with all other charadriiforms, stem and crown clade wing-propelled diving Pan-Alcidae displayed compressed semicircular canals, and indistinct occipital sinuses and cerebellar fissures. Flightless wing-propelled divers have relatively smaller brains for their body mass and smaller optic lobes than volant pan-alcids. Observed differences between volant and flightless wing-propelled sister taxa are striking given that flightless pan-alcids continue to rely on the flight stroke for underwater propulsion. Additionally, the brain of the Black Skimmer Rynchops niger, a taxon with a unique feeding ecology that involves continuous forward aerial motion and touch-based prey detection used both at day and night, is discovered to be unlike that of any other sampled charadriiform in having an extremely large wulst as well as a small optic lobe and distinct occipital sinus. Notably, the differences between the Black Skimmer and other charadriiforms are more pronounced than between wing-propelled divers and other charadriiforms. Finally, aspects of endosseous labyrinth morphology are remarkably similar between divers and non-divers, and may deserve further evaluation.
Project description:The plotopterids (Aves, Plotopteridae) were a group of extinct wing-propelled marine birds that are known from Paleogene-aged sediments (Eocene to Miocene), mostly around the Pacific Rim (especially Japan and the northwest coast of North America). While these birds exhibit a strikingly similar wing morphology to penguins (Spheniscidae), they also share derived characters with pelecaniform birds that are absent in penguins and exhibit apparently superficial similarities with auks (Alcidae: Charadriiformes). Despite quite an abundant fossil record, these birds have been little studied, and in particular their functional morphology remains little understood. Here we present osteological overviews of specimens from the northwest coast of Washington state (USA). We give an amended diagnosis for the well-represented North American genus, Tonsala Olson, 1980, describe a new large species, and examine the functional morphology of plotopterids showing that the ratio of humeral strength to femoral strength is quite low in one well-represented species Tonsala buchanani sp.nov., relative to both extant penguins and alcids. While the femoral strength of Tonsala buchanani is 'penguin-grade', its humeral strength is more 'alcid-grade'. These results have implications for understanding the mode-of-locomotion of these extinct marine birds. Although not related to Spheniscidae, our descriptions and functional results suggest that Tonsala buchanani sustained similar loads in walking, but slightly lower humeral loads during swimming, than a modern penguin. This suggests a swimming mode that is more similar to living alcids, than to the highly-specialised locomotor strategy of living and fossil penguins.
Project description:Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thick-billed murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.
Project description:Although flightless alcids from the Miocene and Pliocene of the eastern Pacific Ocean have been known for over 100 years, there is no detailed evaluation of diversity and systematic placement of these taxa. This is the first combined analysis of morphological and molecular data to include all extant alcids, the recently extinct Great Auk Pinguinus impennis, the mancalline auks, and a large outgroup sampling of 29 additional non-alcid charadriiforms. Based on the systematic placement of Mancallinae outside of crown clade Alcidae, the clade name Pan-Alcidae is proposed to include all known alcids. An extensive review of the Mancallinae fossil record resulted in taxonomic revision of the clade, and identification of three new species. In addition to positing the first hypothesis of inter-relationships between Mancallinae species, phylogenetic results support placement of Mancallinae as the sister taxon to all other Alcidae, indicating that flightlessness evolved at least twice in the alcid lineage. Convergent osteological characteristics of Mancallinae, the flightless Great Auk, and Spheniscidae are summarized, and implications of Mancallinae diversity, radiation, and extinction in the context of paleoclimatic changes are discussed.
Project description:BACKGROUND:Debate regarding the monophyly and relationships of the avian order Pelecaniformes represents a classic example of discord between morphological and molecular estimates of phylogeny. This lack of consensus hampers interpretation of the group's fossil record, which has major implications for understanding patterns of character evolution (e.g., the evolution of wing-propelled diving) and temporal diversification (e.g., the origins of modern families). Relationships of the Pelecaniformes were inferred through parsimony analyses of an osteological dataset encompassing 59 taxa and 464 characters. The relationships of the Plotopteridae, an extinct family of wing-propelled divers, and several other fossil pelecaniforms (Limnofregata, Prophaethon, Lithoptila, ?Borvocarbo stoeffelensis) were also assessed. The antiquity of these taxa and their purported status as stem members of extant families makes them valuable for studies of higher-level avian diversification. METHODOLOGY/PRINCIPAL FINDINGS:Pelecaniform monophyly is not recovered, with Phaethontidae recovered as distantly related to all other pelecaniforms, which are supported as a monophyletic Steganopodes. Some anatomical partitions of the dataset possess different phylogenetic signals, and partitioned analyses reveal that these discrepancies are localized outside of Steganopodes, and primarily due to a few labile taxa. The Plotopteridae are recovered as the sister taxon to Phalacrocoracoidea, and the relationships of other fossil pelecaniforms representing key calibration points are well supported, including Limnofregata (sister taxon to Fregatidae), Prophaethon and Lithoptila (successive sister taxa to Phaethontidae), and ?Borvocarbo stoeffelensis (sister taxon to Phalacrocoracidae). These relationships are invariant when 'backbone' constraints based on recent avian phylogenies are imposed. CONCLUSIONS/SIGNIFICANCE:Relationships of extant pelecaniforms inferred from morphology are more congruent with molecular phylogenies than previously assumed, though notable conflicts remain. The phylogenetic position of the Plotopteridae implies that wing-propelled diving evolved independently in plotopterids and penguins, representing a remarkable case of convergent evolution. Despite robust support for the placement of fossil taxa representing key calibration points, the successive outgroup relationships of several "stem fossil + crown family" clades are variable and poorly supported across recent studies of avian phylogeny. Thus, the impact these fossils have on inferred patterns of temporal diversification depends heavily on the resolution of deep nodes in avian phylogeny.
Project description:Extinct animal behavior has often been inferred from qualitative assessments of relative brain region size in fossil endocranial casts. For instance, flight capability in pterosaurs and early birds has been inferred from the relative size of the cerebellar flocculus, which in life protrudes from the lateral surface of the cerebellum. A primary role of the flocculus is to integrate sensory information about head rotation and translation to stabilize visual gaze via the vestibulo-occular reflex (VOR). Because gaze stabilization is a critical aspect of flight, some authors have suggested that the flocculus is enlarged in flying species. Whether this can be further extended to a floccular expansion in highly maneuverable flying species or floccular reduction in flightless species is unknown. Here, we used micro computed-tomography to reconstruct "virtual" endocranial casts of 60 extant bird species, to extract the same level of anatomical information offered by fossils. Volumes of the floccular fossa and entire brain cavity were measured and these values correlated with four indices of flying behavior. Although a weak positive relationship was found between floccular fossa size and brachial index, no significant relationship was found between floccular fossa size and any other flight mode classification. These findings could be the result of the bony endocranium inaccurately reflecting the size of the neural flocculus, but might also reflect the importance of the flocculus for all modes of locomotion in birds. We therefore conclude that the relative size of the flocculus of endocranial casts is an unreliable predictor of locomotor behavior in extinct birds, and probably also pterosaurs and non-avian dinosaurs.
Project description: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.
Project description:A persistent controversy surrounds the flightless island hen of Tristan da Cunha, Gallinula nesiotis. Some believe that it became extinct by the end of the 19th century. Others suppose that it still inhabits Tristan. There is no consensus about Gallinula comeri, the name introduced for the flightless moorhen from the nearby island of Gough. On the basis of DNA sequencing of both recently collected and historical material, we conclude that G. nesiotis and G. comeri are different taxa, that G. nesiotis indeed became extinct, and that G. comeri now inhabits both islands. This study confirms that among gallinules seemingly radical adaptations (such as the loss of flight) can readily evolve in parallel on different islands, while conspicuous changes in other morphological characters fail to occur.
Project description:The phylogenetic relationships of a number of flightless and volant rails have been investigated using mtDNA sequence data. The third domain of the small ribosomal subunit (12S) has been sequenced for 22 taxa, and part of the 5' end of the cytochrome-b gene has been sequenced for 12 taxa. Additional sequences were obtained from outgroup taxa, two species of jacana, sarus crane, spur-winged plover and kagu. Extinct rails were investigated using DNA extracted from subfossil bones, and in cases where fresh material could not be obtained from other extant taxa, feathers and museum skins were used as sources of DNA. Phylogenetic trees produced from these data have topologies that are, in general, consistent with data from DNA-DNA hybridization studies and recent interpretations based on morphology. Gallinula chloropus moorhen) groups basally with Fulica (coots), Amaurornis (= Megacrex) ineptus falls within the Gallirallus/Rallus group, and Gallinula (= Porphyrula) martinica is basal to Porphyrio (swamphens) and should probably be placed in that genus. Subspecies of Porphyrio porphyrio are paraphyletic with respect to Porphyrio mantelli (takahe). The Northern Hemisphere Rallus aquaticus is basal to the south-western Pacific Rallus (or Gallirallus) group. The flightless Rallus philippensis dieffenbachii is close to Rallus modestus and distinct from the volant Rallus philippensis, and is evidently a separate species. Porzana (crakes) appears to be more closely associated with Porphyrio than Rallus. Deep relationships among the rails remain poorly resolved. Rhynochetus jubatus (kagu) is closer to the cranes than the rails in this analysis. Genetic distances between flightless rails and their volant counterparts varied considerably with observed 12S sequence distances, ranging from 0.3% (Porphyrio porphyrio melanotus and P. mantelli mantelli) to 7.6% (Rallus modestus and Rallus philippensis). This may be taken as an indication of the rapidity with which flightlessness can evolve, and of the persistence of flightless taxa. Genetic data supported the notion that flightless taxa were independently derived, sometimes from similar colonizing ancestors. The morphology of flightless rails is apparently frequently dominated by evolutionary parallelism although similarity of external appearance is not an indication of the extent of genetic divergence. In some cases taxa that are genetically close are morphologically distinct from one another (e.g. Rallus (philippensis) dieffenbachii and R. modestus), whilst some morphologically similar taxa are evidently independently derived (e.g. Porphyio mantelli hochstetteri and P.m. mantelli).
Project description:The recently extinct Malagasy elephant birds (Palaeognathae, Aepyornithiformes) included the largest birds that ever lived. Elephant bird neuroanatomy is understudied but can shed light on the lifestyle of these enigmatic birds. Palaeoneurological studies can provide clues to the ecologies and behaviours of extinct birds because avian brain shape is correlated with neurological function. We digitally reconstruct endocasts of two elephant bird species, Aepyornis maximus and A. hildebrandti, and compare them with representatives of all major extant and recently extinct palaeognath lineages. Among palaeognaths, we find large olfactory bulbs in taxa generally occupying forested environments where visual cues used in foraging are likely to be limited. We detected variation in olfactory bulb size among elephant bird species, possibly indicating interspecific variation in habitat. Elephant birds exhibited extremely reduced optic lobes, a condition also observed in the nocturnal kiwi. Kiwi, the sister taxon of elephant birds, have effectively replaced their visual systems with hyperdeveloped olfactory, somatosensory and auditory systems useful for foraging. We interpret these results as evidence for nocturnality among elephant birds. Vision was likely deemphasized in the ancestor of elephant birds and kiwi. These results show a previously unreported trend towards decreased visual capacity apparently exclusive to flightless, nocturnal taxa endemic to predator-depauperate islands.
Project description:Recent phylogenetic studies question the monophyly of ratites (large, flightless birds incorporating ostriches, rheas, kiwis, emus and cassowaries), suggesting their paraphyly with respect to flying tinamous (Tinamidae). Flightlessness and large body size have thus likely evolved repeatedly among ratites, and separately in ostriches (Struthio) and emus (Dromaius). Here, we test this hypothesis with data from wing developmental trajectories in ostriches, emus, tinamous and chickens. We find the rate of ostrich embryonic wing growth falls within the range of variation exhibited by flying taxa (tinamous and chickens), but that of emus is extremely slow. These results indicate flightlessness was acquired by different developmental mechanisms in the ancestors of ostriches (peramorphosis) and the emu-cassowary clade (paedomorphosis), and corroborate the hypothesis that flight loss has evolved repeatedly among ratites.