Cranial Shape Evolution Research Articles

Skull evolution and lineage diversification in endemic Malagasy carnivorans.

Madagascar is one of the world's foremost biodiversity hotspots with more than 90% of its species endemic to the island. Malagasy carnivorans are one of only four extant terrestrial mammalian clades endemic to Madagascar. Although there are only eight extant species, these carnivorans exhibit remarkable phenotypic and ecological diversity that is often hypothesized to have diversified through an adaptive radiation. Here, we investigated the evolution of skull diversity in Malagasy carnivorans and tested if they exhibited characteristics of convergence and an adaptive radiation. We found that their skull disparity exceeds that of any other feliform family, as their skulls vary widely and strikingly capture a large amount of the morphological variation found across all feliforms. We also found evidence of shared adaptive zones in cranial shape between euplerid subclades and felids, herpestids and viverrids. Lastly, contrary to predictions of adaptive radiation, we found that Malagasy carnivorans do not exhibit rapid lineage diversification and only marginally faster rates of mandibular shape evolution and to a lesser extent cranial shape evolution, compared to other feliforms. These results reveal that exceptional diversification rates are not necessary to generate the striking phenotypic diversity that evolved in carnivorans after their dispersal to and isolation on Madagascar.

Conical and sabertoothed cats as an exception to craniofacial evolutionary allometry

Among evolutionary trends shaping phenotypic diversity over macroevolutionary scales, CREA (CRaniofacial Evolutionary Allometry) describes a tendency, among closely related species, for the smaller-sized of the group to have proportionally shorter rostra and larger braincases. Here, we used a phylogenetically broad cranial dataset, 3D geometric morphometrics, and phylogenetic comparative methods to assess the validity and strength of CREA in extinct and living felids. To test for the influence of biomechanical constraints, we quantified the impact of relative canine height on cranial shape evolution. Our results provided support to CREA at the family level. Yet, whereas felines support the rule, big cats, like Pantherinae and Machairodontinae, conform weakly if not at all with CREA predictions. Our findings suggest that Machairodontinae constitute one of the first well-supported exceptions to this biological rule currently known, probably in response to the biomechanical demands and developmental changes linked with their peculiar rostral adaptations. Our results suggest that the acquisition of extreme features concerning biomechanics, evo-devo constraints, and/or ecology is likely to be associated with peculiar patterns of morphological evolution, determining potential exceptions to common biological rules, for instance, by inducing variations in common patterns of evolutionary integration due to heterochronic changes under ratchet-like evolution.

Mosaic Evolution of the Skull in Labrid Fishes Involves Differences in Both Tempo and Mode of Morphological Change.

Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.].

Cranial shape evolution of extant and fossil crocodile newts and its relation to reproduction and ecology.

The diversity of the vertebrate cranial shape of phylogenetically related taxa allows conclusions on ecology and life history. As pleurodeline newts (the genera Echinotriton, Pleurodeles and Tylototriton) have polymorphic reproductive modes, they are highly suitable for following cranial shape evolution in relation to reproduction and environment. We investigated interspecific differences externally and differences in the cranial shape of pleurodeline newts via two‐dimensional geometric morphometrics. Our analyses also included the closely related but extinct genus Chelotriton to better follow the evolutionary history of cranial shape. Pleurodeles was morphologically distinct in relation to other phylogenetically basal salamanders. The subgenera within Tylototriton (Tylototriton and Yaotriton) were well separated in morphospace, whereas Echinotriton resembled the subgenus Yaotriton more than Tylototriton. Oviposition site choice correlated with phylogeny and morphology. Only the mating mode, with a random distribution along the phylogenetic tree, separated crocodile newts into two morphologically distinct groups. Extinct Chelotriton likely represented several species and were morphologically and ecologically more similar to Echinotriton and Yaotriton than to Tylototriton subgenera. Our data also provide the first comprehensive morphological support for the molecular phylogeny of pleurodeline newts.

A geometric morphometric approach to the analysis of skull shape in Triassic dicynodonts (Therapsida, Anomodontia) from South America.

Dicynodont therapsids were a major component of the Permo-Triassic terrestrial ecosystems across Pangea and have been regarded as specialized herbivores. In South America, the group was represented by several taxa of the clade Kannemeyeriiformes spanning from the Middle to the Late Triassic. In order to evaluate if cranial differences among taxa are potentially related to differences in feeding function, we performed a geometric morphometric analysis on 28 South American dicynodont crania. We digitized 19 cranial landmarks and conducted generalized Procrustes analysis, principal component analysis (PCA), principal component analysis between groups (bg-PCA), and a branch weighted squared-change parsimony approach. Phylogenetic inertia was not a significant driver of cranial shape evolution in the group, whereas PCA and bg-PCA support that major morphological shape differences are concentrated in the preorbital region (relative length of the snout and width of the caniniform process), in the position of quadrate condyle in relation to the caniniform process, and in the increase in the intertemporal surface area. In this context, tusked Dinodontosaurus, "Kannemeyeria," and Vinceria have relatively smaller adductor attachment areas and input moment arm than younger taxa lacking tusks, such as Ischigualastia, Stahleckeria, and Jachaleria. Differences in cranial morphology in later dicynodonts reflect modifications in feeding mechanics, probably due to changes in food resources (vegetation) in their habitats toward the end of the Triassic.

Evolution of cranial shape in a continental-scale evolutionary radiation of Australian lizards.

A defining character of adaptive radiations is the evolution of a diversity of morphological forms that are associated with the use of different habitats, following the invasion of vacant niches. Island adaptive radiations have been thoroughly investigated but continental scale radiations are more poorly understood. Here, we use 52 species of Australian agamid lizards and their Asian relatives as a model group, and employ three-dimensional geometric morphometrics to characterize cranial morphology and investigate whether variation in cranial shape reflects patterns expected from the ecological process of adaptive radiation. Phylogenetic affinity, evolutionary allometry, and ecological life habit all play major roles in the evolution of cranial shape in the sampled lizards. We find a significant association between cranial shapes and life habit. Our results are in line with the expectations of an adaptive radiation, and this is the first time detailed geometric morphometric analyses have been used to understand the selective forces that drove an adaptive radiation at a continental scale.

Crocodylomorph cranial shape evolution and its relationship with body size and ecology.

Crocodylomorpha, which includes living crocodylians and their extinct relatives, has a rich fossil record, extending back for more than 200 million years. Unlike modern semi-aquatic crocodylians, extinct crocodylomorphs exhibited more varied lifestyles, ranging from marine to fully terrestrial forms. This ecological diversity was mirrored by a remarkable morphological disparity, particularly in terms of cranial morphology, which seems to be closely associated with ecological roles in the group. Here, I use geometric morphometrics to comprehensively investigate cranial shape variation and disparity in Crocodylomorpha. I quantitatively assess the relationship between cranial shape and ecology (i.e. terrestrial, aquatic, and semi-aquatic lifestyles), as well as possible allometric shape changes. I also characterize patterns of cranial shape evolution and identify regime shifts. I found a strong link between shape and size, and a significant influence of ecology on the observed shape variation. Terrestrial taxa, particularly notosuchians, have significantly higher disparity, and shifts to more longirostrine regimes are associated with large-bodied aquatic or semi-aquatic species. This demonstrates an intricate relationship between cranial shape, body size and lifestyle in crocodylomorph evolutionary history. Additionally, disparity-through-time analyses were highly sensitive to different phylogenetic hypotheses, suggesting the description of overall patterns among distinct trees. For crocodylomorphs, most results agree in an early peak during the Early Jurassic and another in the middle of the Cretaceous, followed by nearly continuous decline until today. Since only crown-group members survived through the Cenozoic, this decrease in disparity was likely the result of habitat loss, which narrowed down the range of crocodylomorph lifestyles.

Effects of diet on cranial morphology and biting ability in musteloid mammals.

Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size-corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in its entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size-corrected estimated bite force. Many-to-one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size-corrected bite force evolution. Although musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially nonfeeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviours reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial and appendicular form and function with behavioural observations will reveal further insights into the evolution of dietary ecologies and other ecological variables.

Basicranium and face: Assessing the impact of morphological integration on primate evolution

The basicranium and facial skeleton are two integrated structures displaying great morphological diversity across primates. Previous studies focusing on limited taxonomic samples have demonstrated that morphological integration has a significant impact on the evolution of these structures. However, this influence is still poorly understood. A more complete understanding of craniofacial integration across primates has important implications for functional hypotheses of primate evolution. In the present study, we analyzed a large sample of primate species to assess how integration affects the relationship between basicranial and facial evolutionary pathways across the order. First, we quantified integration and modularity between basicranium and face using phylogenetically-informed partial least squares analyses. Then, we defined the influence of morphological integration between these structures on rates of evolution, using a time-calibrated phylogenetic tree, and on disparity through time, comparing the morphological disparity across the tree with that expected under a pure Brownian process. Finally, we assessed the correlation between the basicranium and face, and three factors purported to have an important role in shaping these structures during evolution: endocranial volume, positional behavior (i.e., locomotion and posture), and diet. Our findings show that the face and basicranium, despite being highly integrated, display significantly different evolutionary rates. However, our results demonstrate that morphological integration impacted shape disparity through time. We also found that endocranial volume and positional behavior are important drivers of cranial shape evolution, partly affected by morphological integration.

Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin's finches and Hawaiian honeycreepers.

Adaptive radiation is the rapid evolution of morphologically and ecologically diverse species from a single ancestor. The two classic examples of adaptive radiation are Darwin's finches and the Hawaiian honeycreepers, which evolved remarkable levels of adaptive cranial morphological variation. To gain new insights into the nature of their diversification, we performed comparative three-dimensional geometric morphometric analyses based on X-ray microcomputed tomography (µCT) scanning of dried cranial skeletons. We show that cranial shapes in both Hawaiian honeycreepers and Coerebinae (Darwin's finches and their close relatives) are much more diverse than in their respective outgroups, but Hawaiian honeycreepers as a group display the highest diversity and disparity of all other bird groups studied. We also report a significant contribution of allometry to skull shape variation, and distinct patterns of evolutionary change in skull morphology in the two lineages of songbirds that underwent adaptive radiation on oceanic islands. These findings help to better understand the nature of adaptive radiations in general and provide a foundation for future investigations on the developmental and molecular mechanisms underlying diversification of these morphologically distinguished groups of birds.This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

Suction power output and the inertial cost of rotating the neurocranium to generate suction in fish.

To expand the buccal cavity, many suction-feeding fishes rely on a considerable contribution from dorsal rotation of the dorsal part of the head including the brains, eyes, and several bones forming the braincase and skull roof (jointly referred to as the neurocranium). As the neurocranium takes up a large part of the total mass of the head, this rotation may incur a considerable inertial cost. If so, this would suggest a significant selective pressure on the kinematics and mass distribution of the neurocranium of suction feeders. Here, an inverse dynamic model is formulated to calculate the instantaneous power required to rotate the neurocranium, approximated by a quarter ellipsoid volume of homogeneous density, as well as to calculate the instantaneous suction power based on intra-oral pressure and head volume quantifications. We applied this model to largemouth bass (Micropterus salmoides) and found that the power required to rotate the neurocranium accounts for only about 4% of the power required to suck water into the mouth. Furthermore, recovery of kinetic energy from the rotating neurocranium converted into suction work may be possible during the phase of neurocranial deceleration. Thus, we suggest that only a negligible proportion of the power output of the feeding muscles is lost as inertial costs in the largemouth bass. Consequently, the feeding performance of piscivorous suction feeders with generalised morphology, comparable to our model species, is not limited by neurocranial motion during head expansion. This suggests that it is thus not likely to be a factor of importance in the evolution of cranial shape and size.

Interrelationships Between Bones, Muscles, and Performance: Biting in the Lizard Tupinambis merianae

The origins of and potential constraints on the evolution of phenotypic diversity remain one of the central questions in evolutionary biology. The vertebrate skeleton is governed by historical, developmental, architectural, and functional constraints that all play a role in establishing its final form. Whereas the factors underlying shape variation in single bones are fairly well understood, this is less so the case for complex assemblages of bones as observed in the cranium or mandible. It is often suggested that the final phenotype must reflect the mechanical constraints imposed by the loading of the skeleton as bones remodel to withstand loading. Yet, in the cranium, in contrast to the mandible, the final phenotype is likely constrained by demands other than loading including the protection of sensory systems and the brain. Architectural design constraints may further limit the final form of complex units like the vertebrate cranium. Here we use geometric morphometric approaches to quantify the shape of the cranium and mandible in a lizard and test whether the observed shape co-varies with both the muscles attaching to these structures as well as functional traits such as bite force. Our results show that co-variation between the cranium and mandible is significant and likely driven by the muscles that link the two systems. Moreover, our results show that the patterns of co-variation are stronger between the mandible and ventral side of the cranium. Muscular cross sectional areas, bite force, and the ventral side of the cranium, also co-vary more than the dorsal side of the cranium does with muscle properties and function. Finally, our results show sex-specific patterns of co-variation with males showing a stronger degree of integration between the cranium, mandible, muscles and bite force suggesting that constraints on bite force drive the evolution of cranial shape to a greater extent in males compared to females.

Experimentally induced thermal aseasonality reveals a potential source of variation in Alligator cranial evolution

In the 80 million year evolution, declines in crocodylian diversity correlated with drops in global temperature suggest global temperature is a generative mechanism in crocodylian morphological diversity. Environmentally induced change during development can strongly influence an organism's phenotype. Changes in phenotype in response environment can be broadly referred to as phenotypic plasticity. Alligator mississippiensis ranching provides a unique test of whether seasonality during ontogeny induces cranial shape variability, and if the environmentally induced plasticity corresponds with fossil Alligator evolution. I use 3D geometric morphometrics to analyze extant and fossil Alligator cranial shape. I compare ontogenetic shape change and statistically test for shared ontogenetic shape trajectories; I evaluate patterns of phenotypic evolution, and test for phylogenetic signals in a distribution of shape data. I also present a new software application to visualize 3D morphometric data. Results show the removal of seasonality in Alligator significantly alters cranial shape and shape ontogeny from the wild population. The A. mississippiensis plasticity, climate record, and fossil Alligator cranial shape evolution suggests of a causal link between climate change, ontogeny, and Alligator cranial evolution and insight on rates of evolution of traits in the fossil record.

Do convergent ecomorphs evolve through convergent morphological pathways? Cranial shape evolution in fossil hyaenids and borophagine canids (Carnivora, Mammalia)

Cases of convergent evolution, particularly within ecomorphological contexts, are instructive in identifying universally adaptive morphological features across clades. Tracing of evolutionary pathways by which ecomorphological convergence takes place can further reveal mechanisms of adaptation, which may be strongly influenced by phylogeny. Ecomorphologies of carnivorous mammals represent some of the most outstanding cases of convergent evolution in the Cenozoic radiation of mammals. This study examined patterns of cranial shape change in the dog (Canidae) and hyena (Hyaenidae) families, in order to compare the evolutionary pathways that led to the independent specialization of bone-cracking hypercarnivores within each clade. Geometric morphometrics analyses of cranial shape in fossil hyaenids and borophagine canids provided evidence for deep-time convergence in morphological pathways toward the independent evolution of derived bone-crackers. Both clades contained stem members with plesiomorphic generalist/omnivore cranial shapes, which evolved into doglike species along parallel pathways of shape change. The evolution of specialized bone-crackers from these doglike forms, however, continued under the constraint of a full cheek dentition and restriction on rostrum length reduction in canids, but not hyaenids. Functionally, phylogenetic constraint may have limited borophagine canids to crack bones principally with their carnassial instead of the third premolar as in hyaenids, but other cranial shape changes associated with durophagy nevertheless evolved in parallel in the two lineages. Size allometry was not a major factor in cranial shape evolution in either lineage, supporting the interpretation of functional demands as drivers for the observed convergence. The comparison between borophagines and hyaenids showed that differential effects of alternative functional “solutions” that arise during morphological evolution may be multiplied with processes of the “macroevolutionary ratchet” already in place to further limit the evolutionary pathways available to specialized lineages.

Cranial bone morphometric study among mouse strains

BackgroundLittle is known about the molecular mechanism which regulates how the whole cranium is shaped. Mouse models currently available for genetic research include several hundreds of unique inbred strains and genetically engineered mutants.By cross comparing their genomic structures, we can elucidate the cause of any differences in the phenotype between two strains. The craniometry of subspecies, or closely related species, of mice provide a good systemic model to study the relationship between genetic variance and cranial shape evolution. The lack of a quantified framework for comparing and analyzing mouse cranial shape has been a problem. For this reason, we performed quantitative analysis of cranial shape morphology between several mouse strains.ResultsThis article reports on a craniometric assay of seven mouse strains: four inbred strains (C57BL/6J, BALB/cA, C3H/HeJ, and CBA/JNCr) from Mus musculus domesticus (M. m. domesticus); one closed colony strain (ICR) from M. m. domesticus; one inbred strain (MSM/Ms) from Mus musculus molossinus; and, Mus spretus as a strain from a species other than M. m. domesticus. We performed linear measurements and geometric morphometrics. Geometric morphometrics revealed that the cranial characteristics of each strains were clearly distinguishable. We obtained mean scores for each species using the tpsRelw Program and plotted them.ConclusionGeometric morphometrics proved to be useful for identifying and classifying variations in form, and it revealed that M. spretus has a slender cranium when compared with our other strains. The mean cranial shape of C3H or CBA was more similar to MSM/Ms, which is derived from M. m. molossinus, than to either C57BL/6J, BALB, or ICR which are derived from M. m. domesticus. Future work in this field will aid in elucidating the mechanism of whole cranial shape regulation.

CONVERGENCE AND REMARKABLY CONSISTENT CONSTRAINT IN THE EVOLUTION OF CARNIVORE SKULL SHAPE

Phenotypic similarities between distantly related marsupials and placentals are commonly presented as examples of convergence and support for the role of adaptive evolution in shaping morphological and ecological diversity. Here we compare skull shape in a wide range of carnivoran placentals (Carnivora) and nonherbivorous marsupials using a three-dimensional (3-D) geometric morphometric approach. Morphological and ecological diversity among extant carnivorans is considerably greater than is evident in the marsupial order Dasyuromorphia with which they have most commonly been compared. To examine convergence across a wider, but broadly comparable range of feeding ecologies, a dataset inclusive of nondasyuromorphian marsupials and extinct taxa representing morphotypes no longer present was assembled. We found support for the adaptive paradigm, with correlations between morphology, feeding behavior, and bite force, although skull shape better predicted feeding ecology in the phylogenetically diverse marsupial sample than in carnivorans. However, we also show that remarkably consistent but differing constraints have influenced the evolution of cranial shape in both groups. These differences between carnivorans and marsupials, which correlate with brain size and bite force, are maintained across the full gamut of morphologies and feeding categories, from small insectivores and omnivores to large meat-specialists.