Publications

2026

1. Comparative cranial biomechanics reveal macroevolutionary trends in theropod dinosaurs, with emphasis on Tyrannosauroidea

   Evan Johnson-Ransom, Paul Gignac, Daniel E. Barta, and 2 more authors

   The Anatomical Record, Jan 2026

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   Abstract Tyrannosaurus is viewed as a model organism in vertebrate paleontology, with numerous studies analyzing its feeding biomechanics. Nonetheless, the evolution of this feeding performance has been under-addressed in Tyrannosauroidea, especially in basal tyrannosauroids. Here we used muscle-force reconstruction and finite element analysis (FEA) to quantify the cranial performance of tyrannosauroids and outgroup theropod clades. 2D (planar) cranial models, set to standardized skull lengths and jaw adductor forces, were used to analyze the evolution of feeding behavior in a large sample size of Tyrannosauroidea and other theropods. Sampled stresses matched well between planar and 3D analyses of three disparately shaped crania, suggesting valid interpretations from 2D models along the lateral sides of theropod crania if symmetrical bite loadings are assumed. We traced cranial evolution by sampling stresses at homologous points of theropod crania and input their average stress values into a maximum likelihood ancestral character state estimation. Our results show tyrannosauroids having moderate-to-low cranial stresses. We further tested whether the average stress value correlates with head size through phylogenetic generalized least square regressions. We found that 2D FEA provides significant information on the evolution of feeding performance in a major dinosaur clade. Along internal branches of Tyrannosauroidea, hypothetical common ancestors exhibit low cranial stress values owing to a combination of robust skulls and cranial protuberances. These traits may have been passed down to later tyrannosauroids, enabling them to handle high forces. Our results additionally demonstrate a possible correlation between cranial shape (brevirostrine versus longirostrine) and inferred cranial performance in non-tyrannosauroid clades.

2025

1. Avian cranial evolution is influenced by shape interactions between hard and soft tissue traits

   Andrew Knapp, Taylor West, Catherine M. Early, and 1 more author

   Proceedings of the Royal Society B: Biological Sciences, Dec 2025

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   Changes in the structure and relative size of the brain are thought to be key transformations in the evolution of birds, reflecting innovations and diversity of neurosensory and cognitive capabilities. These changes do not occur in isolation, being accompanied by many other derived morphological characteristics. In the avian head alone, these include the evolution of a toothless beak, an increase in relative eye size, and a reduction and restructuring of jaw muscles. Several developmental trade-offs have been proposed to explain the interrelationships among these traits, but how these developmental patterns translate into evolutionary correlations among cranial traits is poorly understood. Here, we use two-block partial least squares analyses and Ornstein–Uhlenbeck models of adaptive trait evolution to explore the phenotypic evolution of hard and soft cranial tissues and test hypotheses of correlated trait evolution. In pairwise analyses, we found that all traits are significantly correlated, and found support for a form of adaptive trait evolution across the whole head in which traits interact reciprocally via the neurocranium. Together, these results highlight the integrated nature of the avian head and reveal that the evolution of diverse phenotypes is a result of complex multiple interactions among hard and soft tissue traits.

2. Parental Age, Inbreeding and Incubation Method Influence Extremely Low Hatching Success in the Ex‐Situ Population of the Extinct in the Wild Sihek

   Matthew J. Mitchell, Ryan N. Felice, John G. Ewen, and 5 more authors

   Animal Conservation, Jul 2025

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   Low reproductive success rates can be a common problem for threatened species, impacting population viability and limiting recovery potential. Reproductive success can also be particularly low in populations that are managed ex-situ. This can pose a challenge for threatened species recovery programmes because high reproductive success rates are often required to provide offspring for wild releases while ensuring population viability. Understanding the underlying causes of low reproductive success rates in ex-situ populations of threatened species is therefore essential so that management programmes can optimise species’ recovery potential. Here, we quantify rates of egg viability (i.e., indicating fertility and/or early embryo mortality) and total hatching success in the Extinct in the Wild sihek (Guam kingfisher, Todiramphus cinnamominus). Using Bayesian generalised linear mixed models, we investigate effects of parental age, parental inbreeding coefficient ( f), egg f and incubation method on egg viability and hatching success of viable eggs. We find that the sihek population has extremely low egg viability rates (~48% ± 2.15%, N = 304/635) and total egg-hatching success rates (~30% ± 1.82% SE 190/635) compared to other threatened and non-threatened bird species, both ex-situ and in the wild. We find that increased paternal age and f are key drivers of decreased egg viability. In contrast, increased maternal age and use of artificial incubation are important contributors to decreased egg-hatching success. Our results are particularly pertinent given current active recovery planning for sihek, which may require increased offspring production for wild releases. Furthermore, our results suggest that, in closed ex-situ populations where f inevitably increases across generations such that at a given time point older aged individuals may have lower f, there is a need for breeding recommendations to quantitively and systematically balance genetic considerations with species’ biological limitations such as reproductive senescence to meet recovery programme goals.

3. Evolution of growth strategy in alligators and caimans informed by osteohistology of the late Eocene early‐diverging alligatoroid crocodylian Diplocynodon hantoniensis

   D. K. Hoffman, E. R. Goldsmith, A. Houssaye, and 3 more authors

   Journal of Anatomy, Feb 2025

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   Among living crocodylians, alligatoroids exhibit a wide range of body sizes and a biogeographic distribution that spans tropical-to-subtropical climates. The fossil record of alligatoroids, however, reveals even greater diversity, including multiple examples of gigantism and a broader distribution that extends into polar latitudes. Osteohistological studies on extant alligatoroids show that living alligators and caimans both exhibit seasonal growth, with roughly comparable growth rates. However, alligators and caimans diverged from one another over 60 million years ago; the dearth of studies on extinct alligatoroids makes it unclear if the shared condition in extant taxa reflects convergent responses to rapid climatic changes in the recent past or represents the ancestral condition in alligatoroids. Additionally, sample sizes are often limited to one or two individuals, especially in extinct crocodylians, obscuring any intraspecific variation present. To address this uncertainty, we conducted the largest monospecific osteohistological study of an extinct crocodylian to date, based on a sample of nine femora, providing unique insight into the intraspecific variation in growth of the earlydiverging alligatoroid Diplocynodon hantoniensis from the late Eocene of the UK. The bone microanatomy of D. hantoniensis shows moderate compactness, with a welldefined medullary cavity, and osteohistological features that are generally consistent with those of extant alligatoroids. Samples vary greatly along a continuum in the degree of remodelling and vascularity, highlighting both the importance of evaluating intraspecific variation and limitations of basing histological assessments on singleton samples. Ontogenetic assessment indicates that our sample captures a range of skeletally immature to mature individuals, approximately corresponding to femoral size, but with notable exceptions possibly driven by sexual dimorphism. Body size estimates for D. hantoniensis (1.2–3.4 m) fall within the typical range of living American alligators (Alligator mississippiensis). Reconstruction from cyclical growth marks indicates a similar overall growth rate between D. hantoniensis and A. mississippiensis. As in extant alligatoroids more generally, this is determinate, seasonally-controlled growth.

4. The wide gape of snakes: A comparison of the developing mandibular symphysis in sauropsids

   Maricci Basa, Neal Anthwal, Ryan N. Felice, and 1 more author

   Journal of Anatomy, Oct 2025

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   The origin and evolution of snakes has been marked by the acquisition of many morphological and functional novelties, one of which is the possession of a highly kinetic skull allowing for the consumption of prey that are often larger than their head diameter. One feature of the iconic wide gape of macrostomate (large-mouthed) snakes is due to changes in the rostral midline where the left and right hemi-mandible come together. Across vertebrates, the two sides of the lower jaw are held together by the mandibular symphysis. In snakes, the two halves of the lower jaw do not fuse and the symphysis remains free, facilitating gape expansion. The symphysis has previously been explored in lizards and crocodiles, where ligamentous fibres and cartilages span the joint. Here, we compared the anatomy of the forming ‘free’ mandibular symphysis in the corn snake (Pantherophis guttatus) to symphysis development in two lizards, the veiled chameleon (Chamaeleo calyptratus) and the ocelot gecko (Paroedura picta), and an outgroup sauropsid, the chicken (Gallus gallus domesticus). Microcomputed tomography imaging, whole-mount skeletal staining and histology staining confirmed the absence of bone and cartilage fusion at the mandibular symphysis in the corn snake during development, in contrast to the complete fusion of cartilage, but not bone, in both lizards and the fusion of the bone in the chick. Trichrome staining under circular polarised light and whole fast green staining highlighted that, while the symphyseal region was populated by a dense network of collagen fibres, the snake hemi-mandibles were not connected across the rostral region by this fibrous network. Instead, collagen fibres extended backwards and around the snake mental groove to an intermandibular nodule. This nodule attached to the midline dorsally, allowing integration of the movement of the soft and hard tissues. Our analysis highlights the adaptations required to allow extreme lower jaw mobility and independence of the two sides of the jaw as found in macrostomate snakes.

2024

1. Lower jaw modularity in the African clawed frog (Xenopus laevis) and fire salamander (Salamandra salamandra gigliolii)

   Maddison Stevens, Anne-Claire Fabre, and Ryan N Felice

   Biological Journal of the Linnean Society, Oct 2024

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   Abstract Modularity describes the degree to which the components of complex phenotypes vary semi-autonomously due to developmental, genetic and functional correlations. This is a key feature underlying the potential for evolvability, as it can allow individual components to respond to different selective pressures semi-independently. The vertebrate lower jaw has become a model anatomical system for understanding modularity, but to date most of this work has focused on the mandible of mammals and other amniotes. In contrast, modularity in the mandible of lissamphibians has been less well studied. Here, we used geometric morphometrics to quantify the static (intraspecific) modularity patterns in Xenopus laevis and Salamandra salamandra gigliolii. We tested developmental and functional hypotheses of modularity and demonstrate that both species exhibit significant modularity. Functional modularity was supported in both Xenopus and Salamandra. Allometry has a small yet significant impact on lower jaw shape in both taxa and sex has a significant effect on shape in Xenopus. The high lower jaw modularity in both species observed here, combined with the well-established modularity of the amphibian cranium, suggests that modularity is a ubiquitous feature of the tetrapod head.

2023

1. Ecological and life-history drivers of avian skull evolution

   Eloise S E Hunt, Ryan N. Felice, Joseph A Tobias, and 1 more author

   Evolution, Apr 2023

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   One of the most famous examples of adaptive radiation is that of the Galápagos finches, where skull morphology, particularly the beak, varies with feeding ecology. Yet increasingly studies are questioning the strength of this correlation between feeding ecology and morphology in relation to the entire neornithine radiation, suggesting that other factors also significantly affect skull evolution. Here, we broaden this debate to assess the influence of a range of ecological and life-history factors, specifically habitat density, migration, and developmental mode, in shaping avian skull evolution. Using 3D geometric morphometric data to robustly quantify skull shape for 354 extant species spanning avian diversity, we fitted flexible phylogenetic regressions and estimated evolutionary rates for each of these factors across the full data set. The results support a highly significant relationship between skull shape and both habitat density and migration, but not developmental mode. We further found heterogenous rates of evolution between different character states within habitat density, migration, and developmental mode, with rapid skull evolution in species that occupy dense habitats, are migratory, or are precocial. These patterns demonstrate that diverse factors affect the tempo and mode of avian phenotypic evolution and that skull evolution in birds is not simply a reflection of feeding ecology.

2. Developmental origin underlies evolutionary rate variation across the placental skull

   Anjali Goswami, Eve Noirault, Ellen J. Coombs, and 11 more authors

   Philosophical Transactions of the Royal Society B: Biological Sciences, Jul 2023

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   The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull’s major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

3. High-Density Geometric Morphometric Analysis of Intraspecific Cranial Integration in the Barred Grass Snake ( Natrix helvetica ) and Green Anole ( Anolis carolinensis )

   S Tharakan, N Shepherd, D J Gower, and 4 more authors

   Integrative Organismal Biology, Jan 2023

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   Synopsis How do phenotypic associations intrinsic to an organism, such as developmental and mechanical processes, direct morphological evolution? Comparisons of intraspecific and clade-wide patterns of phenotypic covariation could inform how population-level trends ultimately dictate macroevolutionary changes. However, most studies have focused on analyzing integration and modularity either at macroevolutionary or intraspecific levels, without a shared analytical framework unifying these temporal scales. In this study, we investigate the intraspecific patterns of cranial integration in two squamate species: Natrix helvetica and Anolis carolinensis. We analyze their cranial integration patterns using the same high-density three-dimensional geometric morphometric approach used in a prior squamate-wide evolutionary study. Our results indicate that Natrix and Anolis exhibit shared intraspecific cranial integration patterns, with some differences, including a more integrated rostrum in the latter. Notably, these differences in intraspecific patterns correspond to their respective interspecific patterns in snakes and lizards, with few exceptions. These results suggest that interspecific patterns of cranial integration reflect intraspecific patterns. Hence, our study suggests that the phenotypic associations that direct morphological variation within species extend across micro- and macroevolutionary levels, bridging these two scales.

4. The neck as a keystone structure in avian macroevolution and mosaicism

   Ryan D. Marek and Ryan N. Felice

   BMC Biology, Oct 2023

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   Background  The origin of birds from non-avian theropod dinosaur ancestors required a comprehensive restructuring of the body plan to enable the evolution of powered flight. One of the proposed key mechanisms that allowed birds to acquire flight and modify the associated anatomical structures into diverse forms is mosaic evolution, which describes the parcelization of phenotypic traits into separate modules that evolve with heterogeneous tempo and mode. Avian mosaicism has been investigated with a focus on the cranial and appendicular skeleton, and as such, we do not understand the role of the axial column in avian macroevolution. The long, flexible neck of extant birds lies between the cranial and pectoral modules and represents an opportunity to study the contribution of the axial skeleton to avian mosaicism. Results  Here, we use 3D geometric morphometrics in tandem with phylogenetic comparative methods to provide, to our knowledge, the first integrative analysis of avian neck evolution in context with the head and wing and to interrogate how the interactions between these anatomical systems have influenced macroevolutionary trends across a broad sample of extant birds. We find that the neck is integrated with both the head and the forelimb. These patterns of integration are variable across clades, and only specific ecological groups exhibit either head-neck or neckforelimb integration. Finally, we find that ecological groups that display head-neck and neck-forelimb integration tend to display significant shifts in the rate of neck morphological evolution. Conclusions  Combined, these results suggest that the interaction between trophic ecology and head-neck-forelimb mosaicism influences the evolutionary variance of the avian neck. By linking together the biomechanical functions of these distinct anatomical systems, the cervical vertebral column serves as a keystone structure in avian mosaicism and macroevolution.

2022

1. The tempo of cetacean cranial evolution

   Ellen J. Coombs, Ryan N. Felice, Julien Clavel, and 6 more authors

   Current Biology, May 2022

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   The evolution of cetaceans (whales and dolphins) represents one of the most extreme adaptive transitions known, from terrestrial mammals to a highly specialized aquatic radiation that includes the largest animals alive today. Many anatomical shifts in this transition involve the feeding, respiratory, and sensory structures of the cranium, which we quantified with a high-density, three-dimensional geometric morphometric analysis of 201 living and extinct cetacean species spanning the entirety of their 50-million-year evolutionary history. Our analyses demonstrate that cetacean suborders occupy distinct areas of cranial morphospace, with extinct, transitional taxa bridging the gap between archaeocetes (stem whales) and modern mysticetes (baleen whales) and odontocetes (toothed whales). This diversity was obtained through three key periods of rapid evolution: first, the initial evolution of archaeocetes in the early to mid-Eocene produced the highest evolutionary rates seen in cetaceans, concentrated in the maxilla, frontal, premaxilla, and nasal; second, the late Eocene divergence of the mysticetes and odontocetes drives a second peak in rates, with high rates and disparity sustained through the Oligocene; and third, the diversification of odontocetes, particularly sperm whales, in the Miocene ( 18–10 Mya) propels a final peak in the tempo of cetacean morphological evolution. Archaeocetes show the fastest evolutionary rates but the lowest disparity. Odontocetes exhibit the highest disparity, while mysticetes evolve at the slowest pace, particularly in the Neogene. Diet and echolocation have the strongest influence on cranial morphology, with habitat, size, dentition, and feeding method also significant factors impacting shape, disparity, and the pace of cetacean cranial evolution.

2. Attenuated evolution of mammals through the Cenozoic

   Anjali Goswami, Eve Noirault, Ellen J. Coombs, and 11 more authors

   Science, Oct 2022

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   The Cenozoic diversification of placental mammals is the archetypal adaptive radiation. Yet, discrepancies between molecular divergence estimates and the fossil record fuel ongoing debate around the timing, tempo, and drivers of this radiation. Analysis of a three-dimensional skull dataset for living and extinct placental mammals demonstrates that evolutionary rates peak early and attenuate quickly. This long-term decline in tempo is punctuated by bursts of innovation that decreased in amplitude over the past 66 million years. Social, precocial, aquatic, and herbivorous species evolve fastest, especially whales, elephants, sirenians, and extinct ungulates. Slow rates in rodents and bats indicate dissociation of taxonomic and morphological diversification. Frustratingly, highly similar ancestral shape estimates for placental mammal superorders suggest that their earliest representatives may continue to elude unequivocal identification.

2021

1. Cranial integration in the ring-necked parakeet, Psittacula krameri (Psittaciformes: Psittaculidae)

   Matthew J Mitchell, Anjali Goswami, and Ryan N Felice

   Biological Journal of the Linnean Society, Mar 2021

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   Abstract The study of integration and modularity aims to describe the organization of components that make up organisms, and the evolutionary, developmental and functional relationships among them. Both have been studied at the interspecific (evolutionary) and intraspecific (phenotypic and ontogenetic) levels to different degrees across various clades. Although evolutionary modularity and integration are well-characterized across birds, knowledge of intraspecific patterns is lacking. Here, we use a high-density, three-dimensional geometric morphometric approach to investigate patterns of integration and modularity in Psittacula krameri, a highly successful invasive parrot species that exhibits the derived vertical palate and cranio-facial hinge of the Psittaciformes. Showing a pattern of nine distinct cranial modules, our results support findings from recent research that uses similar methods to investigate interspecific integration in birds. Allometry is not a significant influence on cranial shape variation within this species; however, within-module integration is significantly negatively correlated with disparity, with high variation concentrated in the weakly integrated rostrum, palate and vault modules. As previous studies have demonstrated differences in beak shape between invasive and native populations, variation in the weakly integrated palate and rostrum may have facilitated evolutionary change in these parts of the skull, contributing to the ring-necked parakeet’s success as an invasive species.

2. Complex macroevolutionary dynamics underly the evolution of the crocodyliform skull

   Ryan N. Felice, Diego Pol, and Anjali Goswami

   Proceedings of the Royal Society B: Biological Sciences, Jul 2021

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   All modern crocodyliforms (alligators, crocodiles and the gharial) are semi-aquatic generalist carnivores that are relatively similar in cranial form and function. However, this homogeneity represents just a fraction of the variation that once existed in the clade, which includes extinct herbivorous and marine forms with divergent skull structure and function. Here, we use high-dimensional three-dimensional geometric morphometrics to quantify whole-skull morphology across modern and fossil crocodyliforms to untangle the factors that shaped the macroevolutionary history and relatively low phenotypic variation of this clade through time. Evolutionary modelling demonstrates that the pace of crocodyliform cranial evolution is initially high, particularly in the extinct Notosuchia, but slows near the base of Neosuchia, with a late burst of rapid evolution in crown-group crocodiles. Surprisingly, modern crocodiles, especially Australian, southeast Asian, Indo-Pacific species, have high rates of evolution, despite exhibiting low variation. Thus, extant lineages are not in evolutionary stasis but rather have rapidly fluctuated within a limited region of morphospace, resulting in significant convergence. The structures related to jaw closing and bite force production (e.g. pterygoid flange and quadrate) are highly variable, reinforcing the importance of function in driving phenotypic variation. Together, these findings illustrate that the apparent conservativeness of crocodyliform skulls betrays unappreciated complexity in their macroevolutionary dynamics.

2020

1. Decelerated dinosaur skull evolution with the origin of birds

   Ryan N. Felice, Akinobu Watanabe, Andrew R. Cuff, and 6 more authors

   PLOS Biology, Jul 2020

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   The evolutionary radiation of birds has produced incredible morphological variation, including a huge range of skull form and function. Investigating how this variation arose with respect to non-avian dinosaurs is key to understanding how birds achieved their remarkable success after the Cretaceous–Paleogene extinction event. Using a high-dimensional geometric morphometric approach, we quantified the shape of the skull in unprecedented detail across 354 extant and 37 extinct avian and non-avian dinosaurs. Comparative analyses reveal fundamental differences in how skull shape evolved in birds and non-avian dinosaurs. We find that the overall skull shape evolved faster in non-avian dinosaurs than in birds across all regions of the cranium. In birds, the anterior rostrum is the most rapidly evolving skull region, whereas more posterior regions—such as the parietal, squamosal, and quadrate—exhibited high rates in non-avian dinosaurs. These fast-evolving elements in dinosaurs are strongly associated with feeding biomechanics, forming the jaw joint and supporting the jaw adductor muscles. Rapid pulses of skull evolution coincide with changes to food acquisition strategies and diets, as well as the proliferation of bony skull ornaments. In contrast to the appendicular skeleton, which has been shown to evolve more rapidly in birds, avian cranial morphology is characterised by a striking deceleration in morphological evolution relative to non-avian dinosaurs. These results may be due to the reorganisation of skull structure in birds—including loss of a separate postorbital bone in adults and the emergence of new trade-offs with development and neurosensory demands. Taken together, the remarkable cranial shape diversity in birds was not a product of accelerated evolution from their non-avian relatives, despite their frequent portrayal as an icon of adaptive radiations.

2. Metamorphosis shapes cranial diversity and rate of evolution in salamanders

   Anne-Claire Fabre, Carla Bardua, Margot Bon, and 7 more authors

   Nature Ecology and Evolution, Jul 2020

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   Metamorphosis is widespread across the animal kingdom and induces fundamental changes in the morphology, habitat and resources used by an organism during its lifetime. Metamorphic species are likely to experience more dynamic selective pressures through ontogeny compared with species with single-phase life cycles, which may drive divergent evolutionary dynamics. Here, we reconstruct the cranial evolution of the salamander using geometric morphometric data from 148 species spanning the order’s full phylogenetic, developmental and ecological diversity. We demonstrate that life cycle influences cranial shape diversity and rate of evolution. Shifts in the rate of cranial evolution are consistently associated with transitions from biphasic to either direct-developing or paedomorphic life cycle strategies. Direct-developers exhibit the slowest rates of evolution and the lowest disparity, and paedomorphic species the highest. Species undergoing complete metamorphosis (biphasic and direct-developing) exhibit greater cranial modularity (evolutionary independence among regions) than do paedomorphic species, which undergo differential metamorphosis. Biphasic and direct-developing species also display elevated disparity relative to the evolutionary rate for bones associated with feeding, whereas this is not the case for paedomorphic species. Metamorphosis has profoundly influenced salamander cranial evolution, requiring greater autonomy of cranial elements and facilitating the rapid evolution of regions that are remodelled through ontogeny. Rather than compounding functional constraints on variation, metamorphosis seems to have promoted the morphological evolution of salamanders over 180 million years, which may explain the ubiquity of this complex life cycle strategy across disparate organisms.

3. Appendicular skeletal morphology of North American Martes reflect independent modes of evolution in conjunction with Pleistocene glacial cycles

   LM Lynch, Ryan N. Felice, and Haley D O’Brien

   Anatomical Record, Jul 2020

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   Pleistocene glacial cycles are thought to have driven ecological niche shifts, including novel niche formation. North American pine martens, Martes americana and M. caurina, are exemplar taxa thought to have diverged molecularly and morphologically during Pleistocene glaciation. Previous research found correlations between Martes limb morphology with biome and climate, suggesting that appendicular evolution may have occurred via adaptation to selective pressures imposed by novel and shifting habitats. Such variation can also be achieved through non-adaptive means such as genetic drift. Here, we evaluate whether regional genetic differences reflect limb morphology differences among populations of M. americana and M. caurina by analyzing evolutionary tempo and mode of six limb elements. Our comparative phylogenetic models indicate that genetic structure predicts limb shape better than size. Marten limb size has low phylogenetic signal, and the best supported model of evolution is punctuational (kappa), with morphological and genetic divergence occurring simultaneously. Disparity through time analysis suggests that the tempo of limb evolution in Martes tracks Pleistocene glacial cycles, such that limb size may be responding to shifting climates rather than population genetic structure. Contrarily, we find that limb shape is strongly tied to genetic relationships, with high phylogenetic signal and a lambda mode of evolution. Overall, this pattern of limb size and shape variation may be the result of geographic isolation during Pleistocene glacial advance, while declines in disparity suggest hybridization during interglacial periods. Future inclusion of extinct populations of Martes, which were more morphologically and ecologically diverse, may further clarify Martes phenotypic evolution.

4. Late Cretaceous bird from Madagascar reveals unique development of beaks

   Patrick M. O’Connor, Alan H. Turner, Joseph R. Groenke, and 4 more authors

   Nature, Nov 2020

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   Mesozoic birds display considerable diversity in size, flight adaptations and feather organization1–4, but exhibit relatively conserved patterns of beak shape and development5–7. Although Neornithine (that is, crown group) birds also exhibit constraint on facial development8,9, they have comparatively diverse beak morphologies associated with a range of feeding and behavioural ecologies, in contrast to Mesozoic birds. Here we describe a crow-sized stem bird, Falcatakely forsterae gen. et sp. nov., from the Late Cretaceous epoch of Madagascar that possesses a long and deep rostrum, an expression of beak morphology that was previously unknown among Mesozoic birds and is superficially similar to that of a variety of crown-group birds (for example, toucans). The rostrum of Falcatakely is composed of an expansive edentulous maxilla and a small tooth-bearing premaxilla. Morphometric analyses of individual bony elements and three-dimensional rostrum shape reveal the development of a neornithine-like facial anatomy despite the retention of a maxilla–premaxilla organization that is similar to that of nonavialan theropods. The patterning and increased height of the rostrum in Falcatakely reveals a degree of developmental lability and increased morphological disparity that was previously unknown in early branching avialans. Expression of this phenotype (and presumed ecology) in a stem bird underscores that consolidation to the neornithine-like, premaxilla-dominated rostrum was not an evolutionary prerequisite for beak enlargement.

2019

1. Ecomorphological diversification in squamates from conserved pattern of cranial integration

   Akinobu Watanabe, Anne-Claire Fabre, Ryan N. Felice, and 4 more authors

   Proceedings of the National Academy of Sciences, Nov 2019

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   With >10,000 living species, squamate reptiles (lizards, snakes) exhibit enormous phenotypic variation reflecting their incredible range in ecology and developmental strategies. What drove this exceptional diversity? We analyze high-density surface morphometric data for skulls representing ∼200 modern and extinct species to provide a comprehensive, clade-wide investigation of how ecological and developmental factors contributed to cranial evolution across geologic time, skull regions, and taxa. Although diet and habitat have had an overarching impact on skull evolution (e.g., herbivory, along with aquatic and fossorial habitats, are associated with rapid evolution), lizards and snakes surprisingly share a common pattern of trait correlations (integration). The remarkable ecological and morphological diversity in squamates thus arose from selection acting on a conserved architecture of phenotypic integration. Factors intrinsic and extrinsic to organisms dictate the course of morphological evolution but are seldom considered together in comparative analyses. Among vertebrates, squamates (lizards and snakes) exhibit remarkable morphological and developmental variations that parallel their incredible ecological spectrum. However, this exceptional diversity also makes systematic quantification and analysis of their morphological evolution challenging. We present a squamate-wide, high-density morphometric analysis of the skull across 181 modern and extinct species to identify the primary drivers of their cranial evolution within a unified, quantitative framework. Diet and habitat preferences, but not reproductive mode, are major influences on skull-shape evolution across squamates, with fossorial and aquatic taxa exhibiting convergent and rapid changes in skull shape. In lizards, diet is associated with the shape of the rostrum, reflecting its use in grasping prey, whereas snakes show a correlation between diet and the shape of posterior skull bones important for gape widening. Similarly, we observe the highest rates of evolution and greatest disparity in regions associated with jaw musculature in lizards, whereas those forming the jaw articulation evolve faster in snakes. In addition, high-resolution ancestral cranial reconstructions from these data support a terrestrial, nonfossorial origin for snakes. Despite their disparate evolutionary trends, lizards and snakes unexpectedly share a common pattern of trait integration, with the highest correlations in the occiput, jaw articulation, and palate. We thus demonstrate that highly diverse phenotypes, exemplified by lizards and snakes, can and do arise from differential selection acting on conserved patterns of phenotypic integration.

2. High-density morphometric analysis of shape and integration: the good, the bad, and the not-really-a-problem

   Anjali Goswami, Akinobu Watanabe, Ryan N. Felice, and 3 more authors

   Integrative and Comparative Biology, Jun 2019

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   The field of comparative morphology has entered a new phase with the rapid generation of high-resolution three-dimensional (3D) data. With freely available 3D data of thousands of species, methods for quantifying morphology that harness this rich phenotypic information are quickly emerging. Among these techniques, high-density geometric morphometric approaches provide a powerful and versatile framework to robustly characterize shape and phenotypic integration, the covariances among morphological traits. These methods are particularly useful for analyses of complex structures and across disparate taxa, which may share few landmarks of unambiguous homology. However, high-density geometric morphometrics also brings challenges, for example, with statistical, but not biological, covariances imposed by placement and sliding of semilandmarks and registration methods such as Procrustes superimposition. Here, we present simulations and case studies of high-density datasets for squamates, birds, and caecilians that exemplify the promise and challenges of high-dimensional analyses of phenotypic integration and modularity. We assess: (1) the relative merits of “big” high-density geometric morphometrics data over traditional shape data; (2) the impact of Procrustes superimposition on analyses of integration and modularity; and (3) differences in patterns of integration between analyses using high-density geometric morphometrics and those using discrete landmarks. We demonstrate that for many skull regions, 20–30 landmarks and/or semilandmarks are needed to accurately characterize their shape variation, and landmark-only analyses do a particularly poor job of capturing shape variation in vault and rostrum bones. Procrustes superimposition can mask modularity, especially when landmarks covary in parallel directions, but this effect decreases with more biologically complex covariance patterns. The directional effect of landmark variation on the position of the centroid affects recovery of covariance patterns more than landmark number does. Landmark-only and landmark-plus-sliding-semilandmark analyses of integration are generally congruent in overall pattern of integration, but landmark-only analyses tend to show higher integration between adjacent bones, especially when landmarks placed on the sutures between bones introduces a boundary bias. Allometry may be a stronger influence on patterns of integration in landmark-only analyses, which show stronger integration prior to removal of allometric effects compared to analyses including semilandmarks. High-density geometric morphometrics has its challenges and drawbacks, but our analyses of simulated and empirical datasets demonstrate that these potential issues are unlikely to obscure genuine biological signal. Rather, high-density geometric morphometric data exceed traditional landmark-based methods in characterization of morphology and allow more nuanced comparisons across disparate taxa. Combined with the rapid increases in 3D data availability, high-density morphometric approaches have immense potential to propel a new class of studies of comparative morphology and phenotypic integration.

3. Evolutionary Integration and Modularity in the Archosaur Cranium

   Ryan N. Felice, Akinobu Watanabe, Andrew R Cuff, and 6 more authors

   Integrative and Comparative Biology, Jun 2019

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   Complex structures, like the vertebrate skull, are composed of numerous elements or traits that must develop and evolve in a coordinated manner to achieve multiple functions. The strength of association among phenotypic traits (i.e., integration), and their organization into highly-correlated, semi-independent subunits termed modules, is a result of the pleiotropic and genetic correlations that generate traits. As such, patterns of integration and modularity are thought to be key factors constraining or facilitating the evolution of phenotypic disparity by influencing the patterns of variation upon which selection can act. It is often hypothesized that selection can reshape patterns of integration, parceling single structures into multiple modules or merging ancestrally semi-independent traits into a strongly correlated unit. However, evolutionary shifts in patterns of trait integration are seldom assessed in a unified quantitative framework. Here, we quantify patterns of evolutionary integration among regions of the archosaur skull to investigate whether patterns of cranial integration are conserved or variable across this diverse group. Using high-dimensional geometric morphometric data from 3D surface scans and computed tomography scans of modern birds (n = 352), fossil non-avian dinosaurs (n = 27), and modern and fossil mesoeucrocodylians (n = 38), we demonstrate that some aspects of cranial integration are conserved across these taxonomic groups, despite their major differences in cranial form, function, and development. All three groups are highly modular and consistently exhibit high integration within the occipital region. However, there are also substantial divergences in correlation patterns. Birds uniquely exhibit high correlation between the pterygoid and quadrate, components of the cranial kinesis apparatus, whereas the non-avian dinosaur quadrate is more closely associated with the jugal and quadratojugal. Mesoeucrocodylians exhibit a slightly more integrated facial skeleton overall than the other grades. Overall, patterns of trait integration are shown to be stable among archosaurs, which is surprising given the cranial diversity exhibited by the clade. At the same time, evolutionary innovations such as cranial kinesis that reorganize the structure and function of complex traits can result in modifications of trait correlations and modularity.

4. Dietary niche and the evolution of cranial morphology in birds

   Ryan N. Felice, Joseph A Tobias, Alex L Pigot, and 1 more author

   Proceedings of the Royal Society B: Biological Sciences, Jun 2019

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   Cranial morphology in birds is thought to be shaped by adaptive evolution for foraging performance. This understanding of ecomorphological evolution is supported by observations of avian island radiations, such as Darwin’s finches, which display rapid evolution of skull shape in response to food resource availability and a strong fit between cranial phenotype and trophic ecology. However, a recent analysis of larger clades has suggested that diet is not necessarily a primary driver of cranial shape and that phylogeny and allometry are more significant factors in skull evolution. We use phenome-scale morphometric data across the breadth of extant bird diversity to test the influence of diet and foraging behaviour in shaping cranial evolution. We demonstrate that these trophic characters are significant but very weak predictors of cranial form at this scale. However, dietary groups exhibit significantly different rates of morphological evolution across multiple cranial regions. Granivores and nectarivores exhibit the highest rates of evolution in the face and cranial vault, whereas terrestrial carnivores evolve the slowest. The basisphenoid, occipital, and jaw joint regions have less extreme differences among dietary groups. These patterns demonstrate that dietary niche shapes the tempo and mode of phenotypic evolution in deep time, despite a weaker than expected form-function relationship across large clades.

5. A practical guide to sliding and surface semilandmarks in morphometric analyses

   Carla Bardua, Ryan N. Felice, Akinobu Watanabe, and 2 more authors

   Integrative Organismal Biology, Jun 2019

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   Advances in imaging technologies, such as computed tomography (CT) and surface scanning, have facilitated the rapid generation of large datasets of high-resolution 3D specimen reconstructions in recent years. The wealth of phenotypic information available from these datasets has the potential to inform our understanding of morphological variation and evolution. However, the ever-increasing ease of compiling 3D datasets has created an urgent need for sophisticated methods of capturing high-density shape data that reflect the biological complexity in form. Landmarks often do not take full advantage of the rich shape information available from high-resolution 3D specimen reconstructions, as they are typically restricted to sutures or processes that can be reliably identified across specimens and exclude most of the surficial morphology. The development of sliding and surface semilandmark techniques has greatly enhanced the quantification of shape, but their application to diverse datasets can be challenging, especially when dealing with the variable absence of some regions within a structure. Using comprehensive 3D datasets of crania that span the entire clades of birds, squamates and caecilians, we demonstrate methods for capturing morphology across incredibly diverse shapes. We detail many of the difficulties associated with applying semilandmarks to comparable regions across highly disparate structures, and provide solutions to some of these challenges, while considering the consequences of decisions one makes in applying these approaches. Finally, we analyse the benefits of high-density sliding semilandmark approaches over landmark-only studies for capturing shape across diverse organisms and discuss the promise of these approaches for the study of organismal form.

2018

1. Developmental origins of mosaic evolution in the avian cranium

   Ryan N. Felice and Anjali Goswami

   Proceedings of the National Academy of Sciences, Jan 2018

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   Studies reconstructing morphological evolution have long relied on simple representations of organismal form or on limited sampling of species, hindering a comprehensive understanding of the factors shaping biological diversity. Here, we combine high-resolution 3D quantification of skull shape with dense taxonomic sampling across a major vertebrate clade, birds, to demonstrate that the avian skull is formed of multiple semi-independent regions that epitomize mosaic evolution, with cranial regions and major lineages evolving with distinct rates and modes. We further show that the evolvability of different cranial regions reflects their disparate embryonic origins. Finally, we present a hypothetical reconstruction of the ancestral bird skull using this high-resolution shape data to generate a detailed estimate of extinct forms in the absence of well-preserved three-dimensional fossils. Mosaic evolution, which results from multiple influences shaping morphological traits and can lead to the presence of a mixture of ancestral and derived characteristics, has been frequently invoked in describing evolutionary patterns in birds. Mosaicism implies the hierarchical organization of organismal traits into semiautonomous subsets, or modules, which reflect differential genetic and developmental origins. Here, we analyze mosaic evolution in the avian skull using high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highly modular, consisting of seven independently evolving anatomical regions. The face and cranial vault evolve faster than other regions, showing several bursts of rapid evolution. Other modules evolve more slowly following an early burst. Both the evolutionary rate and disparity of skull modules are associated with their developmental origin, with regions derived from the anterior mandibular-stream cranial neural crest or from multiple embryonic cell populations evolving most quickly and into a greater variety of forms. Strong integration of traits is also associated with low evolutionary rate and low disparity. Individual clades are characterized by disparate evolutionary rates among cranial regions. For example, Psittaciformes (parrots) exhibit high evolutionary rates throughout the skull, but their close relatives, Falconiformes, exhibit rapid evolution in only the rostrum. Our dense sampling of cranial shape variation demonstrates that the bird skull has evolved in a mosaic fashion reflecting the developmental origins of cranial regions, with a semi-independent tempo and mode of evolution across phenotypic modules facilitating this hyperdiverse evolutionary radiation.

2. A fly in a tube: macroevolutionary expectations for integrated phenotypes

   Ryan N. Felice, Marcela Randau, and Anjali Goswami

   Evolution, Dec 2018

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   Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium.

2016

1. The evolution of sexually dimorphic tail feathers is not associated with tail skeleton dimorphism

   Ryan N. Felice and Patrick M. O’Connor

   Journal of Avian Biology, May 2016

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   Sexual selection can influence the evolution of sexually dimorphic exaggerated display structures. Herein, we explore whether such costly ornamental integumentary structures evolve independently or if they are correlated with phenotypic change in the associated skeletal system. In birds, elongate tail feathers have frequently evolved in males and are beneficial as intraspecific display structures but impart a locomotor/energetic cost. Using the sexually dimorphic tail feathers of several passeriform species as a model system, we test the hypothesis that taxa with sexually dimorphic tail feathers also exhibit sexual dimorphism in the caudal skeleton that supports the muscles and integument of the tail apparatus. Caudal skeletal morphology is quantified using both geometric morphometrics and linear morphometrics across four sexually dimorphic passeriform species and four closely related monomorphic species. Sexual dimorphism is assessed using permutational MANOVA. Sexual dimorphism in caudal skeletal morphology is found only in those taxa that exhibit active functional differences in tail use between males and females. Thus, dimorphism in tail feather length is not necessarily correlated with the evolution of caudal skeletal dimorphism. Sexual selection is sufficient to generate phenotypic divergence in integumentary display structures between the sexes, but these change are not reflected in the underlying caudal skeleton. This suggests that caudal feathers and bones evolve semi-independently from one another and evolve at different rates in response to different types of selective pressures.

2014

1. Was Ophiacodon (Synapsida, Eupelycosauria) a Swimmer? A Test Using Vertebral Dimensions

   Ryan N. Felice and Kenneth D. Angielczyk

   In Early Evolutionary History of the Synapsida, May 2014

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   Ophiacodon, a Permian synapsid, has been hypothesized to be semi-aquatic. This interpretation is based on a range of evidence, including observations of histology, phalangeal morphology, dentition, and taphonomy. However, many of these data are inconclusive or have been reinterpreted. Here we investigate whether the morphology of the axial skeleton in Ophiacodon displays specializations for aquatic locomotion. Qualitative and quantitative comparisons of Ophiacodon to extant terrestrial and semi-aquatic tetrapods demonstrate that the distribution of centrum lengths in its vertebral column is similar in some ways to those of extant semi-aquatic reptiles. However, other basal synapsids that are widely regarded as terrestrial show comparable patterns, and the correlation between swimming style and vertebral morphology in extant semiaquatic tetrapods may be weaker than previously thought. Therefore, vertebral proportions provide little support for a semi-aquatic lifestyle in Ophiacodon. Given that most lines of evidence are equivocal at best, we suggest that future studies that consider the ecology of Ophiacodon use a terrestrial lifestyle as a null hypothesis.

2. Assessing Trait Covariation and Morphological Integration on Phylogenies Using Evolutionary Covariance Matrices

   Dean C. Adams and Ryan N. Felice

   PLoS ONE, Apr 2014

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   Morphological integration describes the degree to which sets of organismal traits covary with one another. Morphological covariation may be evaluated at various levels of biological organization, but when characterizing such patterns across species at the macroevolutionary level, phylogeny must be taken into account. We outline an analytical procedure based on the evolutionary covariance matrix that allows species-level patterns of morphological integration among structures defined by sets of traits to be evaluated while accounting for the phylogenetic relationships among taxa, providing a flexible and robust complement to related phylogenetic independent contrasts based approaches. Using computer simulations under a Brownian motion model we show that statistical tests based on the approach display appropriate Type I error rates and high statistical power for detecting known levels of integration, and these trends remain consistent for simulations using different numbers of species, and for simulations that differ in the number of trait dimensions. Thus, our procedure provides a useful means of testing hypotheses of morphological integration in a phylogenetic context. We illustrate the utility of this approach by evaluating evolutionary patterns of morphological integration in head shape for a lineage of Plethodon salamanders, and find significant integration between cranial shape and mandible shape. Finally, computer code written in R for implementing the procedure is provided.

3. Ecology and Caudal Skeletal Morphology in Birds: The Convergent Evolution of Pygostyle Shape in Underwater Foraging Taxa

   Ryan N. Felice and Patrick M. O’Connor

   PLoS ONE, Feb 2014

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   Birds exhibit a specialized tail that serves as an integral part of the flight apparatus, supplementing the role of the wings in facilitating high performance aerial locomotion. The evolution of this function for the tail contributed to the diversification of birds by allowing them to utilize a wider range of flight behaviors and thus exploit a greater range of ecological niches. The shape of the wings and the tail feathers influence the aerodynamic properties of a bird. Accordingly, taxa that habitually utilize different flight behaviors are characterized by different flight apparatus morphologies. This study explores whether differences in flight behavior are also associated with variation in caudal vertebra and pygostyle morphology. Details of the tail skeleton were characterized in 51 Aequornithes and Charadriiformes species. Free caudal vertebral morphology was measured using linear metrics. Variation in pygostyle morphology was characterized using Elliptical Fourier Analysis, a geometric morphometric method for the analysis of outline shapes. Each taxon was categorized based on flight style (flap, flap-glide, dynamic soar, etc.) and foraging style (aerial, terrestrial, plunge dive, etc.). Phylogenetic MANOVAs and Flexible Discriminant Analyses were used to test whether caudal skeletal morphology can be used to predict flight behavior. Foraging style groups differ significantly in pygostyle shape, and pygostyle shape predicts foraging style with less than 4% misclassification error. Four distinct lineages of underwater foraging birds exhibit an elongate, straight pygostyle, whereas aerial and terrestrial birds are characterized by a short, dorsally deflected pygostyle. Convergent evolution of a common pygostyle phenotype in diving birds suggests that this morphology is related to the mechanical demands of using the tail as a rudder during underwater foraging. Thus, distinct locomotor behaviors influence not only feather attributes but also the underlying caudal skeleton, reinforcing the importance of the entire caudal locomotor module in avian ecological diversification.

4. Coevolution of caudal skeleton and tail feathers in birds

   Ryan N. Felice

   Journal of Morphology, Dec 2014

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   Birds are capable of a wide range of aerial locomotor behaviors in part because of the derived structure and function of the avian tail. The tail apparatus consists of a several mobile (free) caudal vertebrae, a terminal skeletal element (the pygostyle), and an articulated fan of tail feathers that may be spread or folded, as well as muscular and fibroadipose structures that facilitate tail movements. Morphological variation in both the tail fan and the caudal skeleton that supports it are well documented. The structure of the tail feathers and the pygostyle each evolve in response to functional demands of differing locomotor behaviors. Here, I test whether the integument and skeleton coevolve in this important locomotor module. I quantified feather and skeletal morphology in a diverse sample of waterbirds and shorebirds using a combination of linear and geometric morphometrics. Covariation between tail fan shape and skeletal morphology was then tested using phylogenetic comparative methods. Pygostyle shape is found to be a good predictor of tail fan shape (e.g., forked, graduated), supporting the hypothesis that the tail fan and the tail skeleton have coevolved. This statistical relationship is used to reconstruct feather morphology in an exemplar fossil waterbird, Limnofregata azygosternon. Based on pygostyle morphology, this taxon is likely to have exhibited a forked tail fan similar to that of its extant sister clade Fregata, despite differing in inferred ecology and other aspects of skeletal anatomy. These methods may be useful in reconstructing rectricial morphology in other extinct birds and thus assist in characterizing the evolution of flight control surfaces in birds. J. Morphol. 275:1431–1440, 2014. VC 2014 Wiley Periodicals, Inc.