The effects of skull flattening on suchian jaw muscle evolution.

Jaw muscles are key features of the vertebrate feeding apparatus. The jaw musculature is housed in the skull whose morphology reflects a compromise between multiple functions, including feeding, housing sensory structures, and defense, and the skull constrains jaw muscle geometry. Thus, jaw muscle anatomy may be suboptimally oriented for the production of bite force. Crocodylians are a group of vertebrates that generate the highest bite forces ever measured with a flat skull suited to their aquatic ambush predatory style. However, basal members of the crocodylian line (e.g., Prestosuchus) were terrestrial predators with plesiomorphically tall skulls, and thus the origin of modern crocodylians involved a substantial reorganization of the feeding apparatus and its jaw muscles. Here, we reconstruct jaw muscles across a phylogenetic range of crocodylians and fossil suchians to investigate the impact of skull flattening on muscle anatomy. We used imaging data to create 3D models of extant and fossil suchians that demonstrate the evolution of the crocodylian skull, using osteological correlates to reconstruct muscle attachment sites. We found that jaw muscle anatomy in early fossil suchians reflected the ancestral archosaur condition but experienced progressive shifts in the lineage leading to Metasuchia. In early fossil suchians, musculus adductor mandibulae posterior and musculus pterygoideus (mPT) were of comparable size, but by Metasuchia, the jaw musculature is dominated by mPT. As predicted, we found that taxa with flatter skulls have less efficient muscle orientations for the production of high bite force. This study highlights the diversity and evolution of jaw muscles in one of the great transformations in vertebrate evolution.

Redefining the simplicity of the craniomandibular complex of nightjars: The case of Systellura longirostris (Aves: Caprimulgidae) by means of anatomical network analysis.

To study morphological evolution, it is necessary to combine information from multiple intersecting research fields. Here, we report on the structure of the bony and muscular elements of the craniomandibular complex of birds, highlighting its morphological architecture and complexity (or simplification) in the context of anatomical networks of the Band-winged Nightjar Systellura longirostris (Caprimulgiformes, Caprimulgidae). This species has skull osteology and jaw myology that departs from the general structural plan of the craniomandibular complex of Neornithes and is considered morphologically simple. Our goal is to test if its simplification is also reflected in its anatomical network, particularly in those parameters that measure complexity and to explore if the distribution of the networks in a phylomorphospace is conditioned by their evolutionary history or by convergence. Our results show that S. longirostris clusters with other Strisores and momotids and is segregated from the other bird species analyzed when plotted in the phylomorphospace, as a consequence of convergence in the network parameters. Systellura has a craniomandibular complex consisting of fewer muscles connecting more bones than the model species (e.g., the rock pigeon or the guira cuckoo). In this sense, Systellura is actually more complex regarding the number of integrative bony parts, while its craniomandibular complex is simpler. According to its anatomical network, Systellura also can be interpreted as less complex, particularly compared with other Strisores and taxa that reflect the general structure of the craniomandibular complex in Neornithes.

Biomechanical performance of the cranio-mandibular complex of the small notosuchian Araripesuchus gomesii (Notosuchia, Uruguaysuchidae).

Notosuchia is a clade of crocodyliforms that was highly successful and diverse in the Cretaceous of Gondwana. Araripesuchus gomesii is a small notosuchian from the Early Cretaceous of Brazil that belongs to Uruguaysuchidae, one of the subgroups of notosuchians that first radiated, during the Aptian-Albian. Here we present a finite element analysis of A. gomesii based on a model reconstructed from CT scans and performed using published bone properties for crocodiles. The adductor musculature and their respective attachment areas were reconstructed based on Extant Phylogenetic Bracket. Different functional scenarios were tested applying an estimated 158 N bite force: unilateral bite, bilateral bite, pullback, head-shake, and head-twist. The results obtained were compared with those of Alligator mississippiensis, one of its closest living relatives. In the different simulations, the skull and lower jaws of Araripesuchus suffers more stress in the head-shake movement, followed by the unilateral and pullback bites with stress focalized in the premaxillary region. In contrast, the head-twist is the one with smaller stress values. Araripesuchus possess an oreinirostral skull that may provide greater overall resistance in the different scenarios on average, unlike Alligator that has a platyrostral skull with less resistance to dorsoventral mechanical loads. Previous hypotheses that considered A. gomesii as omnivorous coupled with our results, its small size, and likely limited bite force, suggest this taxon probably fed on small prey and other trophic items that could catch and handle entirely with its mouth, such as insects and small vertebrates.

Unexpected larger distribution of paleogene stem-rollers (AVES, CORACII): new evidence from the Eocene of Patagonia, Argentina.

Here we present the first record of a stem-Coracii outside the Holarctic region, found in the early Eocene of Patagonia at the Laguna del Hunco locality. Ueekenkcoracias tambussiae gen. et sp. nov. consists of an incomplete right hind limb that presents the following combination of characters, characteristic of Coracii: relatively short and stout tibiotarsus, poorly developed crista cnemialis cranialis, short and wide tarsometatarsus, with the tuberositas m. tibialis cranialis located medially on the shaft, and curved and stout ungual phalanges. Although the presence of a rounded and conspicuous foramen vasculare distale and the trochlea metatarsi II strongly deflected medially resemble Primobucconidae, a fossil group only found in the Eocene of Europe and North America, our phylogenetic analysis indicates the new taxon is the basalmost known Coracii. The unexpected presence of a stem-Coracii in the Eocene of South America indicates that this clade had a more widespread distribution than previously hypothesized, already extending into the Southern Hemisphere by the early Eocene. Ueekenkcoracias tambussiae represents new evidence of the increasing diversity of stem lineages of birds in the Eocene. The new material provides novel morphological data for understanding the evolutionary origin and radiation of rollers and important data for estimates of the divergence time of the group.

Tempo and Pattern of Avian Brain Size Evolution.

Relative brain sizes in birds can rival those of primates, but large-scale patterns and drivers of avian brain evolution remain elusive. Here, we explore the evolution of the fundamental brain-body scaling relationship across the origin and evolution of birds. Using a comprehensive dataset sampling> 2,000 modern birds, fossil birds, and theropod dinosaurs, we infer patterns of brain-body co-variation in deep time. Our study confirms that no significant increase in relative brain size accompanied the trend toward miniaturization or evolution of flight during the theropod-bird transition. Critically, however, theropods and basal birds show weaker integration between brain size and body size, allowing for rapid changes in the brain-body relationship that set the stage for dramatic shifts in early crown birds. We infer that major shifts occurred rapidly in the aftermath of the Cretaceous-Paleogene mass extinction within Neoaves, in which multiple clades achieved higher relative brain sizes because of a reduction in body size. Parrots and corvids achieved the largest brains observed in birds via markedly different patterns. Parrots primarily reduced their body size, whereas corvids increased body and brain size simultaneously (with rates of brain size evolution outpacing rates of body size evolution). Collectively, these patterns suggest that an early adaptive radiation in brain size laid the foundation for subsequent selection and stabilization.

The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres).

The extinct dromornithids, gastornithids and phorusrhacids are among the most spectacular birds to have ever lived, with some giants exceeding 500 kg. The affinities and evolution of these and other related extinct birds remain contentious, with previous phylogenetic analyses being affected by widespread convergence and limited taxon sampling. We address these problems using both parsimony and tip-dated Bayesian approaches on an expansive taxon set that includes all key extinct flightless and flighted (e.g. Vegavis and lithornithids) forms, an extensive array of extant fowl (Galloanseres), representative Neoaves and palaeognaths. The Paleogene volant Lithornithidae are recovered as stem palaeognaths in the Bayesian analyses. The Galloanseres comprise four clades inferred to have diverged in the Late Cretaceous on Gondwana. In addition to Anseriformes and Galliformes, we recognize a robust new clade (Gastornithiformes) for the giant flightless Dromornithidae (Australia) and Gastornithidae (Eurasia, North America). This clade exhibits parallels to ratite palaeognaths in that flight presumably was lost and giant size attained multiple times. A fourth clade is represented by the Cretaceous Vegavis (Antarctica), which was strongly excluded from Anseriformes; thus, a crucial molecular calibration point needs to be reconsidered. The presbyornithids Wilaru (Australia) and Presbyornis (Northern Hemisphere) are robustly found to be the sister group to Anatoidea (Anseranatidae + Anatidae), a relatively more basal position than hitherto recognized. South America's largest bird, Brontornis, is not a galloansere, but a member of Neoaves related to Cariamiformes; therefore, giant Galloanseres remain unknown from this continent. Trait analyses showed that while gigantism and flightlessness evolved repeatedly in groups, diet is constrained by phylogeny: all giant Galloanseres and palaeognaths are herbivores or mainly herbivorous, and giant neoavians are zoophagous or omnivorous.

Correction to 'The evolution of giant flightless birds and novel phylogenetic relationships for extinct fowl (Aves, Galloanseres)'.

[This corrects the article DOI: 10.1098/rsos.170975.].

Jaw myology and bite force of the monk parakeet (Aves, Psittaciformes).

Psittaciform birds exhibit novelties in jaw bone structure and musculature that are associated with strong bite forces. These features include an ossified arcus suborbitalis and the muscles ethmomandibularis and pseudomasseter. We analyse the jaw musculature of the monk parakeet (Myiopsitta monachus) to enable future studies aimed at understanding craniofacial development, morphology, function and evolution. We estimate bite force based on muscle dissections, physiological cross-sectional area and skull biomechanical modelling. We also compare our results with available data for other birds and traced the evolutionary origin of the three novel diagnostic traits. Our results indicate that, in Myiopsitta, (i) the arcus suborbitalis is absent and the orbit is ventrally closed by an elongate processus orbitalis and a short ligamentum suborbitale; (ii) the ethmomandibularis muscle is a conspicuous muscle with two bellies, with its origin on the anterior portion of the septum interorbitale and insertion on the medial aspect of the mandible; (iii) the pseudomasseter muscle consists of some fibers arising from the m. adductor mandibulae externus superficialis, covering the lateral surface of the arcus jugalis and attaches by an aponeurotic sheet on the processus orbitalis; (iv) a well-developed adductor mandibulae complex is present; (v) the bite force estimation relative to body mass is higher than that calculated for other non-psittaciform species; and (vi) character evolution analysis revealed that the absence of the arcus suborbitalis and the presence of the m. pseudomassseter are the ancestral conditions, and mapping is inconclusive about presence of one or two bellies of the m. ethmomandibularis.

Skull anatomy of the bizarre crocodylian Mourasuchus nativus (Alligatoridae, Caimaninae).

Mourasuchus is a Miocene alligatorid endemic to South America, and is represented by four species. Together with the closely related Purussaurus, it is a peculiar crocodylian taxon of neogene Caimaninae and one of the most bizarre forms among eusuchian crocodiles. The phylogenetic relationships between Mourasuchus species have not been explored, and detailed skull descriptions are scarce. The goal of this study is to provide new data on skull morphology and cranial recesses in Mourasuchus nativus, including a new tomography analysis (3D modeling). We observed that several diagnostic characters of Purussaurus, such as lack of contact between the nasal and lacrimal, separation of the nasal and frontal by the prefrontals, and the posterior dorsal margin of the skull table, are shared with Mourasuchus. M. nativus is characterized by the presence of solid transverse squamosal eminences, large posttemporal fenestrae, and a quadrate laterocaudal bridge separating V(2) -V(3) trigeminal openings. Compared with other crocodylians, the endocast of M. nativus is similar in shape but quite sigmoid in lateral view, the canal of the supraorbital ramus of V(2) is more vertically oriented, the thick tympanic branch canal opens in a large foramen aligned with trigeminal foramen, and the canal of the vagal (X) tympanic ramus is also very wide. Contrary to extant alligatorids, the median pharyngeal recess remains paired throughout its course and only connects its opposite fellow near the external ventral opening. The knowledge of the internal skull anatomy of Mourasuchus contributes to the understanding of the general morphology of alligatorids, Caimaninae, and their variation.

Flexibility along the neck of the neogene terror bird Andalgalornis steulleti (Aves Phorusrhacidae).

BACKGROUND: Andalgalornis steulleti from the upper Miocene-lower Pliocene (≈6 million years ago) of Argentina is a medium-sized patagornithine phorusrhacid. It was a member of the predominantly South American radiation of 'terror birds' (Phorusrhacidae) that were apex predators throughout much of the Cenozoic. A previous biomechanical study suggests that the skull would be prepared to make sudden movements in the sagittal plane to subdue prey. METHODOLOGY/PRINCIPAL FINDINGS: We analyze the flexion patterns of the neck of Andalgalornis based on the neck vertebrae morphology and biometrics. The transitional cervical vertebrae 5th and 9th clearly separate regions 1-2 and 2-3 respectively. Bifurcate neural spines are developed in the cervical vertebrae 7th to 12th suggesting the presence of a very intricate ligamentary system and of a very well developed epaxial musculature. The presence of the lig. elasticum interespinale is inferred. High neural spines of R3 suggest that this region concentrates the major stresses during downstrokes. CONCLUSIONS/SIGNIFICANCE: The musculoskeletal system of Andalgalornis seems to be prepared (1) to support a particularly big head during normal stance, and (2) to help the neck (and the head) rising after the maximum ventroflexion during a strike. The study herein is the first interpretation of the potential performance of the neck of Andalgalornis in its entirety and we considered this an important starting point to understand and reconstruct the flexion pattern of other phorusrhacids from which the neck is unknown.

Geometric morphometrics of the skull of Tinamidae (Aves, Palaeognathae).

The Tinamidae comprise exclusively Neotropical palaegnathous birds, with homogeneous body morphology and no sexual dimorphism. The goal of this work was to explore the variation in skull morphology between taxa and its possible correspondence with features such as diet or gender using geometric morphometric tools. Eleven landmarks were analyzed in 53 skulls of 4 genera that inhabit grasslands: Nothoprocta, Eudromia, Nothura and Rhynchotus. Intrageneric and intergeneric variability was analyzed. The genera studied here can be distinguished based on the geometric shape of their skull, with prenarial region length and neurocranium shape as the most outstanding features. In the genus Eudromia, males and females could be differentiated, while in the genus Nothoprocta, the species differentiated according to their trophic habits. This study allows establishing that genera and, in some cases, the gender of the Tinamidae can be differentiated based on cranial shape.

Virtual reconstructions of the endocranial cavity of Rhea americana (Aves, Palaeognathae): postnatal anatomical changes.

We examined the external anatomy of the endocast of the Greater Rhea (Rhea americana, Palaeognathae), during 3 main stages of its postnatal life, and compared it with information available on other palaeognathous birds. Series of scans with spiral computed tomographies were obtained from 3 skulls of different ages (chick, juvenile and adult) of R. americana; digital 3-dimensional reconstruction was performed and brain volumes were calculated from the models obtained. Qualitative assessment of the brain anatomy of R. americana indicates a conical and ventrally located bulbus olfactorius, laterally expanded hemispherium telencephali, well-developed eminentia sagittalis, and conspicuous cerebellum and tectum mesencephali. Anatomy of the chick brain was markedly different: less lateral expansion of the hemispherium telencephali, and lesser development of the eminentia sagittalis and auricula cerebelli. Little change between chicks and adults was observed in some brain regions such as the tectum mesencephali, while the eminentia sagittalis showed great increase in size. The large size of the eminentia sagittalis coupled with its increasing development during ontogeny could reflect its importance for visual processing functions and the way these improve during growth. Finally, the brain of R. americana is similar to that of Struthio and Dromaius, but differs from that of the Tinamidae and of Apteryx, allowing recognition of 3 distinct brain morphologies among the Palaeognathae.

Mechanical analysis of feeding behavior in the extinct "terror bird" Andalgalornis steulleti (Gruiformes: Phorusrhacidae).

The South American phorusrhacid bird radiation comprised at least 18 species of small to gigantic terrestrial predators for which there are no close modern analogs. Here we perform functional analyses of the skull of the medium-sized (approximately 40 kg) patagornithine phorusrhacid Andalgalornis steulleti (upper Miocene-lower Pliocene, Andalgalá Formation, Catamarca, Argentina) to assess its mechanical performance in a comparative context. Based on computed tomographic (CT) scanning and morphological analysis, the skull of Andalgalornis steulleti is interpreted as showing features reflecting loss of intracranial immobility. Discrete anatomical attributes permitting such cranial kinesis are widespread phorusrhacids outgroups, but this is the first clear evidence of loss of cranial kinesis in a gruiform bird and may be among the best documented cases among all birds. This apomorphic loss is interpreted as an adaptation for enhanced craniofacial rigidity, particularly with regard to sagittal loading. We apply a Finite Element approach to a three-dimensional (3D) model of the skull. Based on regression analysis we estimate the bite force of Andalgalornis at the bill tip to be 133 N. Relative to results obtained from Finite Element Analysis of one of its closest living relatives (seriema) and a large predatory bird (eagle), the phorusrhacid's skull shows relatively high stress under lateral loadings, but low stress where force is applied dorsoventrally (sagittally) and in "pullback" simulations. Given the relative weakness of the skull mediolaterally, it seems unlikely that Andalgalornis engaged in potentially risky behaviors that involved subduing large, struggling prey with its beak. We suggest that it either consumed smaller prey that could be killed and consumed more safely (e.g., swallowed whole) or that it used multiple well-targeted sagittal strikes with the beak in a repetitive attack-and-retreat strategy.