Jesús Marugán-Lobón

Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context.

Quantifying integration and modularity of evolutionary changes in morphometric traits is crucial for understanding how organismal shapes evolve. For this purpose, comparative studies are necessary, which need to take into account the phylogenetic structure of interspecific data. This study applies several of the standard tools of geometric morphometrics, which mostly have been used in intraspecific studies, in the new context of analyzing integration and modularity based on comparative data. Morphometric methods such as principal component analysis, multivariate regression, partial least squares, and modularity tests can be applied to phylogenetically independent contrasts of shape data. We illustrate this approach in an analysis of cranial evolution in 160 species from all orders of birds. Mapping the shape information onto the phylogeny indicates that there is a significant phylogenetic signal in skull shape. Multivariate regression of independent contrasts of shape on independent contrasts of size reveals clear evolutionary allometry. Regardless of whether or not a correction for allometry is used, evolutionary integration between the face and braincase is strong, and tests reject the hypothesis that the face and braincase are separate evolutionary modules. These analyses can easily be applied to other taxa and can be combined with other morphometric tools to address a wide range of questions about evolutionary patterns and processes.

Birds have paedomorphic dinosaur skulls

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

Life history of a basal bird: morphometrics of the Early Cretaceous Confuciusornis

Confuciusornis sanctus stands out among the remarkable diversity of Mesozoic birds recently unearthed from China. Not only is this primitive beaked pygostylian (birds with abbreviated caudal vertebrae fused into a pygostyle) much more abundant than other avian taxa of this age but differences in plumage between specimens—some having a pair of long stiff tail feathers—have been interpreted as evidence for the earliest example of sexual dimorphism in birds. We report the results of a multivariate morphometric study involving measurements of more than 100 skeletons of C. sanctus. Our analyses do not show any correlation between size distribution and the presence or absence of blade-like rectrices (tail feathers), thus implying, that if these feathers are sexual characters, they are not correlated with sexual size dimorphism. Our results also provide insights into the taxonomy and life history of confuciusornithids, suggesting that these birds may have retained ancestral dinosaurian growth patterns characterized by a midlife exponential growth stage.

Gender identification of the Mesozoic bird Confuciusornis sanctus

Hundreds of specimens of the beaked bird Confuciusornis sanctus have been recovered from Early Cretaceous lake deposits of northeastern China. These birds show remarkable variation in size and plumage, with some displaying two long, central ornamental rectrices (tail feathers) and others lacking them altogether. Although, traditionally specimens with ornamental rectrices were interpreted as males and those without them as females, this supposed sexual dimorphism has remained unconfirmed. Here we report on the discovery of medullary bone, a tissue unique to reproductively active female birds, in a specimen of C. sanctus (DNHM-D1874) lacking these feathers. Our discovery constitutes the first case of gender identification in a Mesozoic bird, and it provides undisputed evidence that individuals of C. sanctus without ornamental rectrices are females. By permitting gender identification in C. sanctus, our results provide insight into the onset of sexual maturity and attainment of adult body size of this and other early birds.

The shapes of bird beaks are highly controlled by nondietary factors

Significance We show that beak and skull shapes in birds of prey (“raptors”) are strongly coupled and largely controlled by size. This relationship means that, rather than being able to respond independently to natural selection, beak shapes are highly constrained to evolve in a particular way. The main aspects of shape variation seem to correspond with specific genes active during development. Because raptors are not each other’s closest relatives, similar shape constraints may therefore have been present in the ancestors of all modern songbirds, including Darwin’s finches, the classic example of explosive evolution in birds. If this hypothesis is true, then such classic examples may be unusual, needing first to break a genetic lock before their beaks could evolve new shapes. Bird beaks are textbook examples of ecological adaptation to diet, but their shapes are also controlled by genetic and developmental histories. To test the effects of these factors on the avian craniofacial skeleton, we conducted morphometric analyses on raptors, a polyphyletic group at the base of the landbird radiation. Despite common perception, we find that the beak is not an independently targeted module for selection. Instead, the beak and skull are highly integrated structures strongly regulated by size, with axes of shape change linked to the actions of recently identified regulatory genes. Together, size and integration account for almost 80% of the shape variation seen between different species to the exclusion of morphological dietary adaptation. Instead, birds of prey use size as a mechanism to modify their feeding ecology. The extent to which shape variation is confined to a few major axes may provide an advantage in that it facilitates rapid morphological evolution via changes in body size, but may also make raptors especially vulnerable when selection pressures act against these axes. The phylogenetic position of raptors suggests that this constraint is prevalent in all landbirds and that breaking the developmental correspondence between beak and braincase may be the key novelty in classic passerine adaptive radiations.

A new specimen of the Early Cretaceous bird Hongshanornis longicresta: insights into the aerodynamics and diet of a basal ornithuromorph

The discovery of Hongshanornis longicresta, a small ornithuromorph bird with unusually long hindlimb proportions, was followed by the discovery of two closely related species, Longicrusavis houi and Parahongshanornis chaoyangensis. Together forming the Hongshanornithidae, these species reveal important information about the early diversity and morphological specialization of ornithuromorphs, the clade that contains all living birds. Here we report on a new specimen (DNHM D2945/6) referable to Hongshanornis longicresta that contributes significant information to better understand the morphology, trophic ecology, and aerodynamics of this species, as well as the taxonomy of the Hongshanornithidae. Most notable are the well-preserved wings and feathered tail of DNHM D2945/6, which afford an accurate reconstruction of aerodynamic parameters indicating that as early as 125 million years ago, basal ornithuromorphs had evolved aerodynamic surfaces comparable in size and design to those of many modern birds, and flight modes alike to those of some small living birds.

Grist for Riedl's mill: a network model perspective on the integration and modularity of the human skull.

Riedls concept of burden neatly links development and evolution by ascertaining that structures that show a high degree of developmental co-dependencies with other structures are more constrained in evolution. The human skull can be precisely modeled as an articulated complex system of bones connected by sutures, forming a network of structural co-dependencies. We present a quantitative analysis of the morphological integration, modularity, and hierarchical organization of this human skull network model. Our overall results show that the human skull is a small-world network, with two well-delimited connectivity modules: one facial organized around the ethmoid bone, and one cranial organized around the sphenoid bone. Geometric morphometrics further support this two-module division, stressing the direct relationship between the developmental information enclosed in connectivity patterns and skull shape. Whereas the facial module shows a hierarchy of clustered blocks of bones, the bones of the cranial modules show a regular pattern of connections. We analyze the significance of these arrangements by hypothesizing specific structural roles for the most important bones involved in the formation of both modules, in the context of Riedls burden. We conclude that it is the morphological integration of each group of bones that defines the semi-hierarchical organization of the human skull, reflecting fundamental differences in the ontogenetic patterns of growth and the structural constraints that generate each module. Our study also demonstrates the adequacy of network analysis as an innovative tool to understand the morphological complexity of anatomical systems.

Structural Constraints in the Evolution of the Tetrapod Skull Complexity: Williston’s Law Revisited Using Network Models

Ever since the appearance of the first land vertebrates, the skull has undergone a simplification by loss and fusion of bones in all major groups. This well-documented evolutionary trend is known as “Williston’s Law”. Both loss and fusion of bones are developmental events that generate, at large evolutionary scales, a net reduction in the number of skull bones. We reassess this evolutionary trend by analyzing the patterns of skull organization captured in network models in which nodes represent bones and links represent suture joints. We also evaluate the compensatory process of anisomerism (bone specialization) suggested to occur as a result of this reduction by quantifying the heterogeneity and the ratio of unpaired bones in real skulls. Finally, we perform simulations to test the differential effect of bone losses in skull evolution. We show that the reduction in bone number during evolution is accompanied by a trend toward a more complex organization, rather than toward simplification. Our results indicate that the processes by which bones are lost or fused during development are central to explain the evolution of the morphology of the skull. Our simulations suggest that the evolutionary trend of increasing morphological complexity can be caused as a result of a structural constraint, the systematic loss of less connected bones during development.

A new crested pterosaur from the early cretaceous of Spain: the first European tapejarid (Pterodactyloidea: Azhdarchoidea)

Background The Tapejaridae is a group of unusual toothless pterosaurs characterized by bizarre cranial crests. From a paleoecological point of view, frugivorous feeding habits have often been suggested for one of its included clades, the Tapejarinae. So far, the presence of these intriguing flying reptiles has been unambiguously documented from Early Cretaceous sites in China and Brazil, where pterosaur fossils are less rare and fragmentary than in similarly-aged European strata. Methodology/Principal Findings Europejara olcadesorum gen. et sp. nov. is diagnosed by a unique combination of characters including an unusual caudally recurved dentary crest. It represents the oldest known member of Tapejaridae and the oldest known toothless pterosaur. The new taxon documents the earliest stage of the acquisition of this anatomical feature during the evolutionary history of the Pterodactyloidea. This innovation may have been linked to the development of new feeding strategies. Conclusion/Significance The discovery of Europejara in the Barremian of the Iberian Peninsula reveals an earlier and broader global distribution of tapejarids, suggesting a Eurasian origin of this group. It adds to the poorly known pterosaur fauna of the Las Hoyas locality and contributes to a better understanding of the paleoecology of this Konservat-Lagerstätte. Finally, the significance of a probable contribution of tapejarine tapejarids to the early angiosperm dispersal is discussed.

Open data and digital morphology

Over the past two decades, the development of methods for visualizing and analysing specimens digitally, in three and even four dimensions, has transformed the study of living and fossil organisms. However, the initial promise that the widespread application of such methods would facilitate access to the underlying digital data has not been fully achieved. The underlying datasets for many published studies are not readily or freely available, introducing a barrier to verification and reproducibility, and the reuse of data. There is no current agreement or policy on the amount and type of data that should be made available alongside studies that use, and in some cases are wholly reliant on, digital morphology. Here, we propose a set of recommendations for minimum standards and additional best practice for three-dimensional digital data publication, and review the issues around data storage, management and accessibility.