Environmental signal in the evolutionary diversification of bird skeletons.

Characterizing how variation in the tempo and mode of evolution has structured the phenotypic diversity of extant species is a central goal of macroevolution1-3. However, studies are typically limited to a handful of traits4-6, providing incomplete information. We analyse morphological diversification in living birds, an ecologically diverse group7, documenting structural scales from 'pan-skeletal' proportions down to the localized three-dimensional shape changes of individual bones. We find substantial variation in evolutionary modes among avian subgroups and among skeletal parts, indicating widespread mosaicism and possible differences in the structure of the macroevolutionary landscape across Earth's main environments. Water-linked groups, especially Aequorlitornithes (waterbirds), have repeatedly explored a large portion of their total morphospace, emphasizing variation in body proportions and in the shape of bones close to the body core, which are functionally related to the mechanics of locomotion8. By contrast, landbirds (Inopinaves) evolved distinct, group-specific body forms early in the aftermath of the K-Pg and subsequently emphasized local shape variation, especially in the head and distal limb bones, which interact more directly with the environment. Passerines, which comprise more than half of all bird species, show a conservative evolutionary dynamic that resulted in low disparity across all skeletal parts. Evidence for early establishment of the morphospace of living birds is clear for some skeletal parts, including beaks and the combined skeletal morphology. However, we find little evidence for early partitioning of that morphospace, contrary to more specific predictions of 'niche-filling' models1,9. Nevertheless, early divergence among broad environmental types may have caused an early divergence of evolutionary modes, suggesting an important role for environmental divergence in structuring the radiation of crown-group birds.

Phylogeny, phylogenetic inference, and cranial evolution in pitheciids and Aotus.

Pitheciids, one of the major radiations of New World monkeys endemic to South and Central America, are distributed in the Amazon and Orinoco basins, and include Callicebus, Cacajao, Chiropotes, and Pithecia. Molecular phylogenetics strongly support pitheciid monophyly, whereas morphological analyses infer a range of phylogenies including a sister relationship between Aotus and Callicebus. We collected geometric morphometric cranial data from pitheciids and Aotus, and used cranial data for distance-based phylogenetic analysis and tests of phylogenetic signal. Phylogenetic analyses of pitheciids were repeated with Lagothrix, Callimico, and Saimiri outgroups for Procrustes shape with and without Aotus based on the whole cranium and six anatomical regions. All phylogenetic signal tests were significant, and tree lengths were shortest and had the least morphological change over the phylogeny for Procrustes residuals from the cranial base and palate. The majority of phylogenetic analyses of Procrustes shape for pitheciids without Aotus supported the molecular phylogeny, and with Aotus included the majority inferred an Aotus-Callicebus clade, although three analyses with Callimico as outgroup supported the molecular phylogeny. The morphological similarity of Aotus and Callicebus is likely a mix of plesiomorphy, allometry, and homoplasy, and future phylogenetic inference of living and extinct platyrrhine taxa should consider the impact of these factors alongside outgroup selection and cranial region.

Earliest evidence for fruit consumption and potential seed dispersal by birds.

The Early Cretaceous diversification of birds was a major event in the history of terrestrial ecosystems, occurring during the earliest phase of the Cretaceous Terrestrial Revolution, long before the origin of the bird crown-group. Frugivorous birds play an important role in seed dispersal today. However, evidence of fruit consumption in early birds from outside the crown-group has been lacking. Jeholornis is one of the earliest-diverging birds, only slightly more crownward than Archaeopteryx, but its cranial anatomy has been poorly understood, limiting trophic information which may be gleaned from the skull. Originally hypothesised to be granivorous based on seeds preserved as gut contents, this interpretation has become controversial. We conducted high-resolution synchrotron tomography on an exquisitely preserved new skull of Jeholornis, revealing remarkable cranial plesiomorphies combined with a specialised rostrum. We use this to provide a near-complete cranial reconstruction of Jeholornis, and exclude the possibility that Jeholornis was granivorous, based on morphometric analyses of the mandible (3D) and cranium (2D), and comparisons with the 3D alimentary contents of extant birds. We show that Jeholornis provides the earliest evidence for fruit consumption in birds, and indicates that birds may have been recruited for seed dispersal during the earliest stages of the avian radiation. As mobile seed dispersers, early frugivorous birds could have expanded the scope for biotic dispersal in plants, and might therefore explain, at least in part, the subsequent evolutionary expansion of fruits, indicating a potential role of bird-plant interactions in the Cretaceous Terrestrial Revolution.

Birds and plants have a close relationship that has developed over millions of years. Birds became diverse and abundant around 135 million years ago. Shortly after, plants started developing new and different kinds of fruits. Today, fruit-eating birds help plants to reproduce by spreading seeds in their droppings. This suggests that birds and plants have coevolved, changing together over time. But it is not clear exactly how their relationship started. One species that might hold the answers is an early bird species known as Jeholornis. It lived in China in the Early Cretaceous, around 120 million years ago. Palaeontologists have discovered preserved seeds inside its fossilised remains. The question is, how did they get there? Some birds eat seeds directly, cracking them open or grinding them up in the stomach to extract the nutrients inside. Other birds swallow seeds when they are eating fruit. If Jeholornis belonged to this second group, it could represent one of the early steps in plant-bird coevolution. Hu et al. scanned and reconstructed a preserved Jeholornis skull and compared it to the skulls, especially the mandibles, of modern birds, including species that grind seeds, species that crack seeds and species that eat fruits, leaving the seeds whole. The analyses ruled out seed cracking. But it could not distinguish between seed grinding and fruit eating. Hu et al. therefore compared the seed remains found inside Jeholornis fossils to seeds eaten by modern birds. The fossilised seeds were intact and showed no evidence of grinding. This suggests that Jeholornis ate whole fruits for at least part of the year. At around the time Jeholornis was alive, the world was entering a phase called the Cretaceous Terrestrial Revolution, which was characterized by an explosion of new species and an expansion of both flowering plants and birds. This finding opens new avenues for scientists to explore how plant and birds might have evolved together. Similar analyses could unlock new information about how other species interacted with their environments.

A methodological investigation of hominoid craniodental morphology and phylogenetics.

The evolutionary relationships of extant great apes and humans have been largely resolved by molecular studies, yet morphology-based phylogenetic analyses continue to provide conflicting results. In order to further investigate this discrepancy we present bootstrap clade support of morphological data based on two quantitative datasets, one dataset consisting of linear measurements of the whole skull from 5 hominoid genera and the second dataset consisting of 3D landmark data from the temporal bone of 5 hominoid genera, including 11 sub-species. Using similar protocols for both datasets, we were able to 1) compare distance-based phylogenetic methods to cladistic parsimony of quantitative data converted into discrete character states, 2) vary outgroup choice to observe its effect on phylogenetic inference, and 3) analyse male and female data separately to observe the effect of sexual dimorphism on phylogenies. Phylogenetic analysis was sensitive to methodological decisions, particularly outgroup selection, where designation of Pongo as an outgroup and removal of Hylobates resulted in greater congruence with the proposed molecular phylogeny. The performance of distance-based methods also justifies their use in phylogenetic analysis of morphological data. It is clear from our analyses that hominoid phylogenetics ought not to be used as an example of conflict between the morphological and molecular, but as an example of how outgroup and methodological choices can affect the outcome of phylogenetic analysis.