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Effects of scaling and locomotor ecology suggest a complex evolution of scapular morphology in sciuromorph rodents
Abstract
Sciuromorph rodents are a monophyletic group comprising ~300 species that display a variety of locomotor behaviours and a body mass range spanning three orders of magnitude. We asked how the interaction of body mass and locomotor ecology affects the morphology of the scapula. Univariate traits and the shape of the scapula from the lateral view of 186 species were analysed. Fitting Ornstein–Uhlenbeck models to all univariate traits revealed phylogenetic inertia to be low. Hence, ordinary least squares regressions including an interaction term were used for all traits to test whether the scaling relationships differ in the fossorial and aerial groups when compared with the group characterized by arboreal locomotion, the most probable ancestral sciuromorph condition. We also asked whether the scaling of univariate traits departs from isometry in each of the three locomotor groups. The aerial group was expected to show the highest trait values for a given body mass and the highest slope values, followed by the arboreal and fossorial groups along this sequence. Only a few traits showed a difference in scaling among locomotor groups and/or a distinct allometric pattern. Discrepancies between our expectations and results are discussed in a morphofunctional context.
... Our results are congruent with previous studies showing a low or negligible allometric effect on scapular shape variation of small eutherian mammals, such as bats (Gaudioso et al. 2020) and sciuromorph (Wölfer et al. 2019) and caviomorph rodents (Morgan 2009). Even in sciuromorph rodents, where this effect is shown to be somewhat more pronounced than in bats and caviomorphs, only 8.4% of the total variation in scapular shape is explained by variation in body mass (see Table S3 in Wölfer et al. 2019). ...
... Our results are congruent with previous studies showing a low or negligible allometric effect on scapular shape variation of small eutherian mammals, such as bats (Gaudioso et al. 2020) and sciuromorph (Wölfer et al. 2019) and caviomorph rodents (Morgan 2009). Even in sciuromorph rodents, where this effect is shown to be somewhat more pronounced than in bats and caviomorphs, only 8.4% of the total variation in scapular shape is explained by variation in body mass (see Table S3 in Wölfer et al. 2019). The allometric effect on the scapula of didelphid marsupials is greater than that found in the eutherian small mammals, being more pronounced in larger species (Astúa 2009). ...
... The infraspinous fossa tends to be disproportionately more expanded in didelphids of greater body mass (Astúa 2009). Unlike didelphids, echimyids, as well as other caviomorph and sciuromorph rodents (Morgan 2009;Wölfer et al. 2019), tend to have a relationship between body size and infraspinous and supraspinous fossae sizes close to isometric. All these observations suggest absence of a generalized and conserved allometric pattern in the scapula of small therian mammals, although further studies are needed to verify this hypothesis. ...
Locomotion, as a fundamental function in mammals directly associated with the use of ecological resources, is expected to have anatomical structures functionally committed that evolved under intense selective pressure, possibly carrying specializations for different locomotor habits. Among caviomorph rodents, the family Echimyidae stands out for having the greatest species richness, with relatively well-resolved phylogenetic relationships, wide variation in body mass, and remarkable diversity of locomotor habits, including arboreal, scansorial, semi-aquatic, semifossorial, and terrestrial forms. Thus, Echimyidae constitutes a promising model for understanding how phylogenetic, allometric, and ecological factors affect the evolution of postcranial structures directly linked to locomotor function. We investigated the influence of these three factors on scapular and humeral morphological variation in 38 echimyid species using two-dimensional geometric morphometry and phylogenetically informed comparative methods. Scapular and humeral shape variation had a low correlation with body mass and structure size, conveying a small or negligible allometric effect. Conversely, a significant moderate to strong phylogenetic signal was detected in both structures, suggesting that an important part of their morphometric variation results from shared evolutionary history. Notably, morphological variation of the scapula was extensively structured by phylogeny, without the marked influence of locomotor habits, suggesting that its shape may be a suitable taxonomic marker. Finally, locomotor habits were important in structuring the morphological variation of the humerus. Our results suggest that the morphologies of the scapula and humerus, despite being anatomically and functionally interconnected, were differentially shaped by ecological factors associated with locomotor habits.
Goodwin's brush‐tailed mouse ( Calomyscus elburzensis Goodwin, 1939) is a poorly known small rodent that occupies rocky habitats in Iran, Turkmenistan, Afghanistan, Pakistan, Azerbaijan, and Syria. Herein, a detailed description of the shape, size, and function of the postcranial skeleton of this species is presented for the first time. Trapping was carried out in eastern Iran between the years 2013 and 2015. Skeletal parts of 24 adult male specimens were removed using the papain digestion protocol, and several postcranial morphological characteristics and measurements were examined. We attempted to achieve a morpho‐functional characterization of Goodwin's brush‐tailed mouse and to match morphological specializations with previous information on the ecology, behavior, and phylogenetic inferences of this rodent. Goodwin's brush‐tailed mouse has extended transverse processes and long zygapophyses in the first five caudal vertebrae along with a good innervation of the caudal vertebrae, which has resulted in a well‐developed basal musculature of the tail. It has extended forelimb, long ilium, and short post‐acetabular part of the innominate bone, loose hip joint with high degree of lateral movement of the hindlimb, and long distal elements of the hindlimb. These features have resulted in fast terrestrial movements in open microhabitats, including climbing and jumping. Although superficial scratching of the ground is observed, the species is incapable of digging burrows. Evaluation of postcranial morphological characteristics and character states further indicated the basal radiation of the genus Calomyscus among other Muroidea. Findings constitute a source of information for morpho‐functional and phylogenetic comparisons between Calomyscidae and other mouse‐like muroids.
Many of the squirrel‐related rodents (i.e., Sciuromorpha) are tree‐dwelling species known to be very agile climbers. This taxon also includes the most diverse clade of gliding (aerial) mammals that likely descended from a non‐gliding arboreal ancestor and evolved a patagium (i.e., a gliding membrane) to increase gliding performance. Glides can cover distances of up to 150 m and landing is typically accomplished by stalling the patagium to reduce impact velocity. It remains unclear if this behavior suffices to keep stresses on the locomotor apparatus similar to those experienced by their arboreal relatives or whether gliding behavior increases landing forces and stresses. The sparsely available support reaction force data are ambiguous, but bone microstructure is highly adaptable to changes in loading regime and likely provides insights into this question. Using μCT scans, we compared the cortical thickness of the glenoid fossa of the shoulder joint between arboreal and aerial Sciuromorpha using evolutionary model comparison, while also accounting for regional differences of the glenoid fossa. We did not find any differences between these locomotor behaviors, irrespective of the glenoid region. These findings agree with previous analyses of the microstructure of the femur in Sciuromorpha. We discuss different aspects that could explain the similarity in cortical thickness. According to our analysis of glenoid cortical thickness the loading regime appears not to have changed after the evolution of gliding locomotion, likely due to adjustments in landing performance.
Homoplasy is a strong indicator of a phenotypic trait's adaptive significance when it can be linked to a similar function. We assessed homoplasy in functionally relevant scapular and femoral traits of Marmotini and Xerini, two sciuromorph rodent clades that independently acquired a fossorial lifestyle from an arboreal ancestor. We studied 125 species in the scapular dataset and 123 species in the femoral dataset. Pairwise evolutionary model comparison was used to evaluate whether homoplasy of trait optima is more likely than other plausible scenarios. The most likely trend of trait evolution among all traits was assessed via likelihood scoring of all considered models. The homoplasy hypothesis could never be confirmed as the single most likely model. Regarding likelihood scoring, scapular traits most frequently did not differ among Marmotini, Xerini, and arboreal species. For the majority of femoral traits, results indicate that Marmotini, but not Xerini, evolved away from the ancestral arboreal condition. We conclude on the basis of the scapular results that the forelimbs of fossorial and arboreal sciuromorphs share mostly similar functional demands, whereas the results on the femur indicate that the hind limb morphology is less constrained, perhaps depending on the specific fossorial habitat.
Homoplasy is a strong indicator of a phenotypic trait's adaptive significance when it can be linked to a similar function. We assessed homoplasy in functionally relevant scapular and femoral traits of Marmotini and Xerini, two sciuromorph rodent clades that independently acquired a fossorial lifestyle from an arboreal ancestor. We studied 125 species in the scapular dataset and 123 species in the femoral dataset. Pairwise evolutionary model comparison was used to evaluate whether homoplasy of trait optima is more likely than other plausible scenarios. The most likely trend of trait evolution among all traits was assessed via likelihood scoring of all considered models. The homoplasy hypothesis could never be confirmed as the single most likely model. Regarding likelihood scoring, scapular traits most frequently did not differ among Marmotini, Xerini, and arboreal species. For the majority of femoral traits, results indicate that Marmotini, but not Xerini, evolved away from the ancestral arboreal condition. We conclude on the basis of the scapular results that the forelimbs of fossorial and arboreal sciuromorphs share mostly similar functional demands, whereas the results on the femur indicate that the hind limb morphology is less constrained, perhaps depending on the specific fossorial habitat. This study is concerned with the scapular and femoral trait evolution in sciuromorph rodents with an emphasis on trait homoplasy between two fossorial lineages, Marmotini and Xerini. Evolutionary model comparison does not suggest homoplasy to be a likely scenario. Instead, it appears that the scapula is more conserved, reflecting the ancestral arboreal condition, whereas the femoral morphology shifted away from this condition in Marmotini, but not in Xerini.
Sciuromorph rodents are a monophyletic group comprising about 300 species with a body mass range spanning three orders of magnitude and various locomotor behaviors that we categorized into arboreal, fossorial and aerial. The purpose of this study was to investigate how the interplay of locomotor ecology and body mass affects the morphology of the sciuromorph locomotor apparatus. The most proximal skeletal element of the hind limb, i.e. the femur, was selected, because it was shown to reflect a functional signal in various mammalian taxa. We analyzed univariate traits (effective femoral length, various robustness variables and the in‐levers of the muscles attaching to the greater, third and lesser trochanters) as well as femoral shape, representing a multivariate trait. An ordinary least‐squares regression including 177 species was used to test for a significant interaction effect between body mass and locomotor ecology on the variables. Specifically, it tested whether the scaling patterns of the fossorial and aerial groups differ when compared with the arboreal, because the latter was identified as the ancestral sciuromorph condition via stochastic character mapping. We expected aerial species to display the highest trait values for a given body mass as well as the steepest slopes, followed by the arboreal and fossorial species along this order. An Ornstein–Uhlenbeck regression fitted to a phylogenetically pruned dataset of 140 species revealed the phylogenetic inertia to be very low in the univariate traits, hence justifying the utilization of standard regressions. These variables generally scaled close to isometry, suggesting that scaling adjustments might not have played a major role for most of the femoral features. Nevertheless, the low phylogenetic inertia indicates that the observed scaling patterns needed to be maintained during sciuromorph evolution. Significant interaction effects were discovered in the femoral length, the centroid size of the condyles, and the in‐levers of the greater and third trochanters. Additionally, adjustments in various femoral traits reflect the acquisitions of fossorial and aerial behaviors from arboreal ancestors. Using sciuromorphs as a focal clade, our findings exemplify the importance of statistically accounting for potential interaction effects of different environmental factors in studies relating morphology to ecology.
Background
Bone structure has a crucial role in the functional adaptations that allow vertebrates to conduct their diverse lifestyles. Much has been documented regarding the diaphyseal structure of long bones of tetrapods. However, the architecture of trabecular bone, which is for instance found within the epiphyses of long bones, and which has been shown experimentally to be extremely plastic, has received little attention in the context of lifestyle adaptations (virtually only in primates). We therefore investigated the forelimb epiphyses of extant xenarthrans, the placental mammals including the sloths, anteaters, and armadillos. They are characterised by several lifestyles and degrees of fossoriality involving distinct uses of their forelimb. We used micro computed tomography data to acquire 3D trabecular parameters at regions of interest (ROIs) for all extant genera of xenarthrans (with replicates). Traditional, spherical, and phylogenetically informed statistics (including the consideration of size effects) were used to characterise the functional signal of these parameters.
Results
Several trabecular parameters yielded functional distinctions. The main direction of the trabeculae distinguished lifestyle categories for one ROI (the radial trochlea). Among the other trabecular parameters, it is the degree of anisotropy (i.e., a preferential alignment of the trabeculae) that yielded the clearest functional signal. For all ROIs, the armadillos, which represent the fully terrestrial and fossorial category, were found as characterised by a greater degree of anisotropy (i.e., more aligned trabeculae). Furthermore, the trabeculae of the humeral head of the most fossorial armadillos were also found to be more anisotropic than in the less fossorial species.
Conclusions
Most parameters were marked by an important intraspecific variability and by a size effect, which could, at least partly, be masking the functional signal. But for some parameters, the degree of anisotropy in particular, a clear functional distinction was recovered. Along with data on primates, our findings suggest that a trabecular architecture characterised by a greater degree of anisotropy is to be expected in species in which the relevant epiphyses withstand a restricted range of load directions. Trabecular architecture therefore is a promising research avenue for the reconstruction of lifestyles in extinct or cryptic species.
Electronic supplementary material
The online version of this article (10.1186/s12983-017-0241-x) contains supplementary material, which is available to authorized users.
Anatomical traits associated with locomotion often exhibit specializations for ecological niche, suggesting that locomotor specializations may constitute selective regimes acting on limb skeletal traits. To test this, I sampled 42 species of Mustelidae, encompassing climbing, digging, and swimming specialists, and determined whether trait variation reflects locomotor specialization by performing a principal components analysis on 14 forelimb traits. In addition to Brownian motion models, three Ornstein–Uhlenbeck models of selective regimes were applied to PC scores describing trait variation among mustelids: one without a priori defined phenotypic optima, one with optima based upon locomotor habit, and one with a single phenotypic optimum. PC1, which explained 43.8% of trait variance, represented a trade-off in long bone gracility and deltoid ridge length vs. long robustness and olecranon process length and distinguished between climbing specialists and remaining mustelids. PC2, which explained 17.4% of trait variance, primarily distinguished the sea otter from other mustelids. Best fitting trait diversification models are selective regimes differentiating between scansorial and nonscansorial mustelids (PC1) and selective regimes distinguishing the sea otter and steppe polecat from remaining mustelids (PC2). Phylogenetic half-life values relative to branch lengths suggest that, in spite of a strong rate of adaptation, there is still the influence of past trait values. However, simulations of likelihood ratios suggest that the best fitting models are not fully adequate to explain morphological diversification within extant mustelids.
Recent years have seen increased interest in phylogenetic comparative analyses of multivariate datasets, but to date the varied proposed approaches have not been extensively examined. Here we review the mathematical properties required of any multivariate method, and specifically evaluate existing multivariate phylogenetic comparative methods in this context. Phylogenetic comparative methods based on the full multivariate likelihood are robust to levels of covariation among trait dimensions and are insensitive to the orientation of the dataset, but display increasing model misspecification as the number of trait dimensions increases. This is because the expected evolutionary covariance matrix (V) used in the likelihood calculations becomes more ill-conditioned as trait dimensionality increases, and as evolutionary models become more complex. Thus, these approaches are only appropriate for datasets with few traits and many species. Methods that summarize patterns across trait dimensions treated separately (e.g., SURFACE) incorrectly assume independence among trait dimensions, resulting in nearly a 100% model misspecification rate. Methods using pairwise composite likelihood are highly sensitive to levels of trait covariation, the orientation of the dataset, and the number of trait dimensions. The consequences of these debilitating deficiencies is that a user can arrive at differing statistical conclusions, and therefore biological inferences, simply from a dataspace rotation, like principal component analysis. By contrast, algebraic generalizations of the standard phylogenetic comparative toolkit that use the trace of covariance matrices are insensitive to levels of trait covariation, the number of trait dimensions, and the orientation of the dataset. Further, when appropriate permutation tests are used, these approaches display acceptable Type I error and statistical power. We conclude that methods summarizing information across trait dimensions, as well as pairwise composite likelihood methods should be avoided, while algebraic generalizations of the phylogenetic comparative toolkit provide a useful means of assessing macroevolutionary patterns in multivariate data. Finally, we discuss areas in which multivariate phylogenetic comparative methods are still in need of future development; namely highly multivariate Ornstein-Uhlenbeck models and approaches for multivariate evolutionary model comparisons.
Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints not only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.
The shape of long bones is linked to a species’ ecology and is thought to reflect the constraints imposed by locomotion. The evolution of the shape of the long bones in semi-aquatic mustelids has likely been shaped by the divergent mechanical properties of both water and land. Adaptation to a semi-aquatic lifestyle occurred independently in otters (Lutrinae) and minks (Mustelinae). Here we test the idea that these similar locomotor constraints led to morphological convergence between minks and otters, and between European and American minks. We use 3D geometric morphometrics to quantify shape differences in the humerus, radius, ulna, femur, tibia and fibula of ten species of mustelids belonging to the Lutrinae and Mustelinae subfamilies. Our results show convergence in all bones between the European and American minks, but this convergence is significant only for the humerus. We suggest that this strong convergence in humeral shape between the two minks results from functional demands on the forelimb as it produces most of the thrust when swimming in minks. The American minks show a slight but nonsignificant convergence with the Lutrinae for the shape of the ulna, femur and tibia. The sea otter (Enhydra lutris) shows an ulnar and radial shape that diverges from that observed in the other Lutrinae, possibly due to the strong manipulative abilities and unique locomotor mode of this species. In contrast to our initial hypothesis, bone shape in minks does not converge significantly with that of otters. Otters show a large variety of shapes suggesting that a semi-aquatic lifestyle can comprise a wide array of locomotor behaviours.
Squirrels of the World, written by scientists with more than 100 years of collective experience studying these popular mammals, is the first comprehensive examination of all 285 species of squirrels worldwide. The authors reveal virtually every detail of the family Sciuridae, which includes ground squirrels, tree squirrels, flying squirrels, prairie dogs, and chipmunks. Each species-from the familiar gray squirrel of American backyards to the exotic and endangered woolly flying squirrel of Pakistan-is described in a detailed account that includes distinguishing characteristics, ecology, natural history, conservation status, and current threats to its existence. Squirrels of the World includes · stunning color photographs that document rare and unusual squirrels as well as common varieties · evolution, morphology, ecology, and conservation status · colorful range maps marking species distribution · images of the skull of each genus of squirrel · extensive references. © 2012 The Johns Hopkins University Press. All rights reserved.
Animals that glide produce aerodynamic forces that enable transit through the air in both arboreal and aquatic environments. The relative ease of gliding compared with flapping flight has led to a large diversity of taxa that have evolved some degree of flight capability. Glide paths are curved, reflecting the changing forces on the animal as it progresses through its aerial trajectory. These changing forces can be under control of the glider, which uses specific aspects of anatomy to modulate lift, drag, and rotational moments on the body. However, gliders share no single anatomical or behavioral feature, and some species are unspecialized for gliding, producing aerodynamic forces using posture and orientation alone. Animals use gliding in a broad range of ecological roles, suggesting that multiple performance metrics are relevant for consideration, but we are only beginning to understand how gliders produce and control their flight from takeoff to landing. In this review, we focus on the physical aspects of how glide trajectories are produced, and additionally discuss the range of morphologies and postures that are used to control aerial movements across the broad diversity of animal gliders.
Flying squirrels range in length of head and body from less than 90 mm to more than 400 mm. Large flying squirrels are more slender than tree squirrels or small flying squirrels. They have proportionately longer tails than small flying squirrels, but large tree squirrels have the longest tails of all, both absolutely and proportionately. Relative limb lengths decrease with size among flying and tree squirrels, but the ratio of forelimb to hindlimb length is generally higher for flying squirrels than for tree squirrels. The styliform cartilage adds to the area of the patagium, but it is isometric with respect to size. Weight varies by a factor of almost 64 and the area of the patagium by a factor of almost 16, with little divergence from the expected isometric relationship. Therefore “wing loading” varies almost by a factor of four and is estimated to be as low as 30 Newtons/square meter (N/m2) in small petauristines and as great as 110 N/m2 in large ones.
Hang gliding seems to provide a good analogue for the gliding of flying squirrels, although the squirrels have lower aspect ratios (l.0 to 2.2) and lower glide ratios (less than 3) than do most hang gliders. From this analogy it seems probable that the heavier “wing loading” of large flying squirrels does not affect the glide ratio (horizontal distance/vertical drop) but that the larger flying squirrels must “fly” faster to maximize their glide ratio. It is also probable that small flying squirrels with lower “wing loadings” are more maneuverable, but large flying squirrels with heavier loadings are less affected by air turbulence.
Genomic data are rapidly resolving the tree of living species calibrated to time, the timetree of life, which will provide a framework for research in diverse fields of science. Previous analyses of taxonomically restricted timetrees have found a decline in the rate of diversification in many groups of organisms, often attributed to ecological interactions among species. Here we have synthesized a global timetree of life from 2,274 studies representing 50,632 species and examined the pattern and rate of diversification as well as the timing of speciation. We found that species diversity has been mostly expanding overall and in many smaller groups of species, and that the rate of diversification in eukaryotes has been mostly constant. We also identified, and avoided, potential biases that may have influenced previous analyses of diversification including low levels of taxon sampling, small clade size, and the inclusion of stem branches in clade analyses. We found consistency in time-to-speciation among plants and animals-approximately two million years-as measured by intervals of crown and stem species times. Together, this clock-like change at different levels suggests that speciation and diversification are processes dominated by random events and that adaptive change is largely a separate process.
© The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Photographic and videographic investigations of the aerodynamic performance of four captive adult Acrobates pygmeus are described. During short (1–4 m) glides, steep angles of descent (>45 degrees) and large angles of attack (up to 50 degrees) were used mid-flight, and the possums failed to achieve steady velocities. During longer (>10 m) glides steady velocities of 5.3–7.5 ms–1 were achieved, and glide angles of 21–42 degrees and angles of attack between 36 and 45 degrees were used. The best (lowest) glide angles used at steady velocity were similar to those documented in sugar gliders, but involved lower air speeds. During steady gliding the forelimbs of Acrobates assumed an ‘elbows-out’ disposition similar to that of Petauroides volans, and unlike that of petaurid gliders. A glide polar for Acrobates shows that it uses lower air speeds and higher sinking speeds than other gliding animals for which polars are available (several birds and one bat). Few data on the radius of turn and sinking speed were obtained; nevertheless, in accord with theory, sinking speeds were higher during tighter turns. During flight the feather-like tail was used to generate pitching movements and adjust the angle of attack and hence glide angle. However, the control of turns seems to be achieved primarily through limb adjustments.
In this study, three-dimensional landmark-based methods of geometric morphometrics are used for estimating the influence of phylogeny, allometry and locomotor performance on forelimb shape in living and extinct carnivorans (Mammalia, Carnivora). The main objective is to investigate morphological convergences towards similar locomotor strategies in the shape of the major forelimb bones. Results indicate that both size and phylogeny have strong effects on the anatomy of all forelimb bones. In contrast, bone shape does not correlate in the living taxa with maximum running speed or daily movement distance, two proxies closely related to locomotor performance. A phylomorphospace approach showed that shape variation in forelimb bones mainly relates to changes in bone robustness. This indicates the presence of biomechanical constraints resulting from opposite demands for energetic efficiency in locomotion -which would require a slender forelimb- and resistance to stress -which would be satisfied by a robust forelimb-. Thus, we interpret that the need of maintaining a trade-off between both functional demands would limit shape variability in forelimb bones. Given that different situations can lead to one or another morphological solution, depending on the specific ecology of taxa, the evolution of forelimb morphology represents a remarkable "one-to-many mapping" case between anatomy and ecology.
For squirrels, physical size varies with ancestry, locomotion, and sex. Body length has little variation associated with subfamilies or tribes but varies significantly among genera within tribes. Thus, patterns in body size among genera represent more recent evolutionary pressures. Flying squirrels weigh less than similarly sized tree or ground squirrels but ecological profile and ancestry are confounded for flying squirrels. Tail length has clear relationships with ecological profile in squirrels. Tail length is shorter in ground squirrels, longer in tree squirrels, and longest in flying squirrels. In addition, in arboreal squirrels, females have longer tails, relative to body length, than those of males. This latter result suggests that reproductive constraints can influence external features of morphology.
Many ecological and evolutionary studies seek to explain patterns of shape variation and its covariation with other variables. Geometric morphometrics is often used for this purpose, where a set of shape variables are obtained from landmark coordinates following a P rocrustes superimposition.
We introduce geomorph: a software package for performing geometric morphometric shape analysis in the r statistical computing environment.
Geomorph provides routines for all stages of landmark‐based geometric morphometric analyses in two and three‐dimensions. It is an open source package to read, manipulate, and digitize landmark data, generate shape variables via P rocrustes analysis for points, curves and surfaces, perform statistical analyses of shape variation and covariation, and to provide graphical depictions of shapes and patterns of shape variation. An important contribution of geomorph is the ability to perform P rocrustes superimposition on landmark points, as well as semilandmarks from curves and surfaces.
A wide range of statistical methods germane to testing ecological and evolutionary hypotheses of shape variation are provided. These include standard multivariate methods such as principal components analysis, and approaches for multivariate regression and group comparison. Methods for more specialized analyses, such as for assessing shape allometry, comparing shape trajectories, examining morphological integration, and for assessing phylogenetic signal, are also included.
Several functions are provided to graphically visualize results, including routines for examining variation in shape space, visualizing allometric trajectories, comparing specific shapes to one another and for plotting phylogenetic changes in morphospace.
Finally, geomorph participates to make available advanced geometric morphometric analyses through the r statistical computing platform.
The scapula of the ecomorphologically diverse South American caviomorph rodents was studied through geometric morphometric techniques, using landmarks and semilandmarks to capture the shape of this complex morphological structure. Representatives of 33 species from all caviomorph superfamilies, as well as Hystrix cristata for comparisons, were analyzed. Marked differences in scapular shape were found among the major caviomorph lineages analyzed, particularly in the shape and length of the scapular spine and development of the great scapular notch. Shape differences were not influenced by body size, and only partially influenced by locomotor mode. Thus, at this scale of analysis, phylogenetic history seems to be the strongest factor influencing scapular shape. The scapular shape of erethizontids, chinchillids and Cuniculus paca could represent the less specialized state with respect to the highly differentiated scapula of octodontoids and most cavioids. In this sense, the characteristic scapular morphologies of octodontoids and cavioids could reflect particular functional capabilities and constraints associated with the evolution of prevalent locomotor modes within each lineage.
Superimposition methods for comparing configurations of landmarks in two or more specimens are reviewed. These methods show
differences in shape among specimens as residuals after rotation, translation, and scaling them so that they align as well
as possible. A new method is presented that generalizes Siegel and Benson's (1982) resistant-fit theta-rho analysis so that
more than two objects can be compared at the same time. Both least-squares and resistant-fit approaches are generalized to
allow for affine transformations (uniform shape change). The methods are compared, using artificial data and data on 18 landmarks
on the wings of 127 species of North American mosquitoes. Graphical techniques are also presented to help summarize the patterns
of differences in shape among the objects being compared.
Optimisation of energy by aquatic mammals requires adaptations that reduce drag, and improve thrust production and efficiency. Drag is minimised by streamlining the body and appendages. Highly derived aquatic mammals have body shapes close to the optimal hydrodynamic design for drag reduction. There is no conclusive evidence for specialised drag reduction mechanisms, although decreasing hair density is associated with reduced drag. Improvement in thrust production and efficiency is accomplished by changes in propulsive mode and appendage design. Semiaquatic mammals employ drag-based propulsion using paddles, whereas fully aquatic mammals use lift-based propulsion with hydrofoils. Because paddling generates thrust through half the stroke cycle, propulsive efficiency is low and energetic cost is high compared with that for mammals using hydrofoils. Lift-based swimming is a rapid and high-powered propulsive mode. Oscillations of the hydrofoil generate thrust throughout the stroke cycle. For cetaceans and pinnipeds, propulsive efficiency is approximately 80%, and transport cost is below that of semiaquatic mammals. Behavioural adaptations help minimise energy expenditure by swimming mammals. Submerged swimming avoids increased drag from energy lost in formation of surface waves. Porpoising and wave riding, characteristic of dolphins, can reduce the transport costs, allowing for longer-duration swimming at high speeds.
Background
Development of phylogenetic methods that do not rely on fossils for the study of evolutionary processes through time have revolutionized the field of evolutionary biology and resulted in an unprecedented expansion of our knowledge about the tree of life. These methods have helped to shed light on the macroevolution of many taxonomic groups such as the placentals (Mammalia). However, despite the increase of studies addressing the diversification patterns of organisms, no synthesis has addressed the case of the most diversified mammalian clade: the Rodentia.
Results
Here we present a rodent maximum likelihood phylogeny inferred from a molecular supermatrix. It is based on 11 mitochondrial and nuclear genes that covers 1,265 species, i.e., respectively 56% and 81% of the known specific and generic rodent diversity. The inferred topology recovered all Rodentia clades proposed by recent molecular works. A relaxed molecular clock dating approach provided a time framework for speciation events. We found that the Myomorpha clade shows a greater degree of variation in diversification rates than Sciuroidea, Caviomorpha, Castorimorpha and Anomaluromorpha. We identified a number of shifts in diversification rates within the major clades: two in Castorimorpha, three in Ctenohystrica, 6 within the squirrel-related clade and 24 in the Myomorpha clade. The majority of these shifts occurred within the most recent familial rodent radiations: the Cricetidae and Muridae clades. Using the topological imbalances and the time line we discuss the potential role of different diversification factors that might have shaped the rodents radiation.
Conclusions
The present glimpse on the diversification pattern of rodents can be used for further comparative meta-analyses. Muroid lineages have a greater degree of variation in their diversification rates than any other rodent group. Different topological signatures suggest distinct diversification processes among rodent lineages. In particular, Muroidea and Sciuroidea display widespread distribution and have undergone evolutionary and adaptive radiation on most of the continents. Our results show that rodents experienced shifts in diversification rate regularly through the Tertiary, but at different periods for each clade. A comparison between the rodent fossil record and our results suggest that extinction led to the loss of diversification signal for most of the Paleogene nodes.
Sigmodontinae rodents constitute the second-largest subfamily among mammals. Alongside the taxonomic diversity, they are also ecologically diverse, exhibiting a wide array of locomotion modes, with semifossorial, terrestrial, semiaquatic, scansorial, arboreal, and saltatorial forms. To understand the ecomorphologic aspects that allow these rodents to display such locomotion diversity, we analyzed 35 qualitative characters of the appendicular skeleton (humerus, ulna, radius, scapula, femur, tibia, ilium, ischium and pubis) in 795 specimens belonging to 64 species, 34 genera and 10 tribes, representing all locomotion modes assigned to this subfamily. We performed a statistical analysis based upon the coefficient of trait differentiation to test the congruence of character states and the different locomotion modes. We also mapped characters states in a molecular phylogeny in order to reconstruct ancestral states and to evaluate how appendicular characters evolved within main lineages of Sigmodontinae radiation under a phylogenetic framework. The statistical analyses revealed six characters related to specific locomotion modes, except terrestrial. The mapping and parsimony ancestral states reconstruction identified two characters with phylogenetical signal and eight characters that are exclusively or more frequently recorded in certain modes of locomotion, four of them also detected by the statistical analysis. Notwithstanding the documented morphological variation, few changes characterize the transition to each of the locomotion modes, at least regarding the appendicular skeleton. This finding corroborates previous results that showed that sigmodontines exhibit an all-purpose appendicular morphology that allows them to use and explore a great variety of habitats.
The mathematical/statistical software platform R has seen an immense increase in popularity within the last decade. Its main advantages are its flexibility, a large repository of freely available extensions, its open-source nature and a thriving community. This tutorial gives an introduction into landmark/surface-mesh based statistical shape analysis in R – specifically using the packages Morpho and Rvcg . Beginning with examples based on sparse sets of anatomical landmarks, the tutorial will go on dealing with surface and curve landmarks and more challenging tasks such as mesh manipulations and surface registration. Apart from statistical analyses, emphasis will also be put on comprehensive visualization of the results. Extensive examples and code snippets are provided to allow the reader to easily replicate the analyses.
Morphometrics, a new branch of statistics, combines tools from geometry, computer graphics and biometrics in techniques for the multivariate analysis of biological shape variation. Although medical image analysts typically prefer to represent scenes by way of curving outlines or surfaces, the most recent developments in this associated statistical methodology have emphasized the domain of landmark data: size and shape of configurations of discrete, named points in two or three dimensions. This paper introduces a combination of Procrustes analysis and thin-plate splines, the two most powerful tools of landmark-based morphometrics, for multivariate analysis of curving outlines in samples of biomedical images. The thin-plate spline is used to assign point-to-point correspondences, called semi-landmarks, between curves of similar but variable shape, while the standard algorithm for Procrustes shape averages and shape coordinates is altered to accord with the ways in which semi-landmarks formally differ from more traditional landmark loci. Subsequent multivariate statistics and visualization proceed mainly as in the landmark-based methods. The combination provides a range of complementary filters, from high pass to low pass, for effects on outline shape in grouped studies. The low-pass version is based on the spectrum of the spline, the high pass, on a familiar special case of Procrustes analysis. This hybrid method is demonstrated in a comparison of the shape of the corpus callosum from mid-sagittal sections of MRI of 25 human brains, 12 normal and 13 with schizophrenia.
1. We present mvMORPH, a package of multivariate phylogenetic comparative methods for the R statistical environment. mvMORPH is freely available on the CRAN package repository (http://cran.r-project.org/web/packages/mvMORPH/).
2. mvMORPH allows fitting a range of multivariate evolutionary models under a maximum-likelihood criterion. Initially developed in the context of phylogenetic analysis of multiple morphometric traits, its use can be extended to any biological dataset with one or multiple covarying continuous traits. All the fitting models include the possibility to use SIMMAP-like mapping, which may be useful for fitting changes along lineages at a given point in time. All models provide diagnostic metrics for convergence and reliability of estimates, as well as the possibility to include trait measurement errors in model estimates.
3. New features provided by the mvMORPH package include the possibility of fitting models with changes in the mode of evolution along the phylogeny, which will be particularly meaningful in comparative analyses that include extinct taxa, e.g., when testing changes in evolutionary mode associated with global biotic/abiotic events.
4. We briefly describe the models already included in mvMORPH, and provide some demonstration of the use of the package with two simulated worked examples.
Convergence in morphology can result from evolutionary adaptations in species living in environments with similar selective pressures. Here, we investigate whether the shape of the forelimb long bones has converged in environments imposing similar functional constraints, using musteloid carnivores as a model. The limbs of quadrupeds are subjected to many factors that may influence their shape. They need to support body mass without collapsing or breaking, yet at the same time resist the stresses and strains induced by locomotion. This likely imposes strong constraints on their morphology. Our geometric morphometric analyses show that locomotion, body mass and phylogeny all influence the shape of the forelimb. Furthermore, we find a remarkable convergence between: (i) aquatic and semi-fossorial species, both displaying a robust forelimb, with a shape that improves stability and load transfer in response to the physical resistance imposed by the locomotor environment; and (ii) aquatic and arboreal/semi-arboreal species, with both groups displaying a broad capitulum. This augments the degree of pronation/supination, an important feature for climbing as well as grasping and manipulation ability, behaviors common to aquatic and arboreal species. In summary, our results highlight how musteloids with different locomotor ecologies show differences in the anatomy of their forelimb bones. Yet, functional demands for limb movement through dense media also result in convergence in forelimb long-bone shape between diverse groups, for example, otters and badgers.
© 2015 Anatomical Society.
Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per-lineage speciation rates, species richness, disparity and a time-invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
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1. Here, I present a new, multifunctional phylogenetics package, phytools, for the R statistical computing environment.
2. The focus of the package is on methods for phylogenetic comparative biology; however, it also includes tools for tree inference, phylogeny input/output, plotting, manipulation and several other tasks.
3. I describe and tabulate the major methods implemented in phytools, and in addition provide some demonstration of its use in the form of two illustrative examples.
4. Finally, I conclude by briefly describing an active web-log that I use to document present and future developments for phytools. I also note other web resources for phylogenetics in the R computational environment.
This book is about the importance of animal size. We tend to think of animal function in chemical terms and talk of water, salts, proteins, enzymes, oxygen, energy, and so on. We should not forget, however, that physical laws are equally important, for they determine rates of diffusion and heat transfer, transfer of force and momentum, the strength of structures, the dynamics of locomotion, and other aspects of the functioning of animal bodies. Physical laws provide possibilities and opportunities for an organism, yet they also impose constraints, setting limits to what is physically possible. This book aims to give an understanding of these rules because of their profound implications when we deal with animals of widely different size and scale. The reader will find that the book raises many questions. Remarkable and puzzling information makes it read a little like a detective story, but the last chapter, instead of giving the final solution, neither answers all questions nor provides one great unifying principle.
Sigmodontine rats are one of the most diverse components of the Neotropical mammal fauna. They exhibit a wide ecological diversity and a variety of locomotor types that allow them to occupy different environments. To explore the relationship between morphology and locomotor types, we analyzed traits of the postcranial osteology (axial and appendicular skeletons) of 329 specimens belonging to 51 species and 29 genera of sigmodontines exhibiting different locomotor types. In this work, postcranial skeletal characters of these rats are considered in an ecomorphological study for the first time. Statistical analyses showed that of the 34 osteological characters considered, 15 were related to the locomotor types studied, except for ambulatory. However, character mapping showed that climbing and jumping sigmodontines are the only taxa exhibiting clear adaptations in their postcranial osteology, which are highly consistent with the tendencies described in many other mammal taxa. Climbing, digging and swimming rats presented statistically differences in traits associated with their vertebral column and limbs, whereas jumping rats showed modifications associated with all the skeletal regions. Our data suggest that sigmodontine rats retain an all-purpose morphology that allows them to use a variety of habitats. This versatility is particularly important when considering the lack of specialization of sigmodontines for a specific locomotor mode. Another possible interpretation is that our dataset probably did not consider relevant information about these groups and should be increased with other types of characters (e.g. characters from the external morphology, myology, etc.).
Two sets of anatomical data are presented for six marsupial genera from French Guyana: tissue (skin, muscle, bone) and organ (alimentary tract, brain, eyes) proportions, and segmental distribution of mass (head, tail, thighs, etc.). As a percentage of total weight, skin is about equal in all genera, but the percentage of muscle is low in Caluromys and Didelphis (32%) and exceptionally high in Metachirus (45%); the percentage of viscera is low in Marmosa (6%) and high in Caluromys (10%). Philander, Caluromys, and Marmosa are similar in the segmental distribution of weight: large head, moderately sized thighs, and heavy, prehensile tail. Caluromys and Philander differ in the percentage of total muscle, size of the eyes, and weight of the alimentary tract. Only Monodelphis and Metachirus strongly diverge from the group, and Metachirus possesses many characteristics of high-speed terrestrial cursors such as Dolichotis and Lepus: high percentage of muscle in the body; muscular arms and thighs; elongated and lightened feet; and heavy lumbar extensor muscles. Basically, however, the Didelphidae remain small, prehensile-tailed, scampering and climbing omnivores with only moderate hindlimb dominance. They have not differentiated structurally as much as the prosimians in comparable niches in West Africa or Madagascar. Certain forces have acted conservatively upon body size and locomotor tissues.
The cineradiographic study of the locomotion of the rock hyrax (Procavia capensis) and the functional interpretation of its locomotory system, reveals that the main action of proximal segments is combined with flexed position and low movements of limb joints. This observation can be applied to the locomotion of other small mammals. In the forelimb, scapular rotation and translation account for more than 60% of step length. Effective shoulder joint movements are mostly restricted to less than 20°, and elbow movements range mainly between 20°-50°. The detachment of the shoulder girdle of therian mammals from the axial skeleton, and development of a supraspinous fossa, are correlated with movements at a high scapular fulcrum. Movements at such a high fulcrum are in interdependency with a crouched posture. Only flexed limbs can act as shock absorbers and prevent vertical changes in the center of gravity. Basic differences in forelimb movements exist between larger primates (humeral retraction) and smaller mammals (scapula retraction). In the hyrax, propulsion is due mainly to hip joint movements in symmetrical gaits, but sagittal lumbar spine movements play the dominant role at inphase gaits. Joint and muscular anatomy, especially of the shoulder region, are discussed in view of the kinematic data.
Die Untersuchungen sowohl der äußeren Gestalt als ouch der Muskulatur der Vorder- und Hinterextremität haben gezeigt, daß die vier Nagetiere, Eichhörnchen, Murmeltier, Biber and Hase Typen ver schiedener Anpassungsrichtungen darstellen. Dabei ist auffallend, daß die einzelnen Arten nicht nur in ihren allgemeinen Proportionen, sondern auch in Einzelheiten der Muskelausbildung den angehörigen anderer Ordnungen ähnlich sind (Konvergenz). Das Eichhörnchen, nähert sich den gut springenden Affen, der Biber den Robben and der Hase den Huftieren.
South American caviomorph rodents comprise four major lineages encompassing wide taxonomic and ecological diversity, but the morphological diversity of their postcranial skeleton has not been thoroughly explored using phylogenetic comparative methods. The main goal of this work is to analyze their humerus using geometric morphometrics in a phylogenetic context and attempt to tease apart the influence of locomotory preferences and shared evolutionary history on morphological variation. We examined 28 genera in 9 families representing all major clades. Humeral shape was captured by 13 landmarks and four semilandmarks in 2D. In the morphospace of the first two principal components, most taxa were located near the origin along both axes. Fossorial octodontoids were apart from this central group. Most caviids were separated in one extreme of the morphospace; the specialized digging ctenomyid Ctenomys, the fossorial chinchillid Lagostomus and the generalized cavioid Cuniculus were located at the opposite end. Phylogenetic signal was significant. Regressions of shape on size were not significant; regression of shape on habit was significant for raw data and not significant after phylogenetic control. Humeral shape variation was primarily associated with the phylogenetic structure of the group; additionally, some morphological traits were associated with particular habits and interpreted as functional specializations. This association between humeral shape and both phylogeny and habit at different hierarchical levels suggests early ecomorphological diversification of caviomorphs.
Rodents of the subfamily Sigmodontinae comprise a highly diversified group in the Atlantic Forest, with semifossorial, terrestrial, semiaquatic, scansorial, and arboreal forms. In this study, we analyzed morphometric variation in humerus, scapula, ulna, radius, femur, tibia, and pelvis to investigate its possible relationship with the different types of locomotion recorded in the literature. Skeletal characters were measured in 321 specimens belonging to 29 species and 19 genera either restricted to or recorded in this ecoregion. Multivariate morphometric analyses (principal component and canonical variate analyses) arranged individuals of different genera in groups congruent with the different types of locomotion. This arrangement was more clearly defined when analyses included only forelimb measurements, indicating that most of the variation in appendicular traits associated with the different locomotor modes occurs in the forelimb skeleton. Semifossorial forms exhibited the most distinct appendicular morphology, as well as the greatest frequency of endemism among analyzed species. These results suggest that this mode of locomotion led to greater differentiation in semifossorial Atlantic forest sigmodontines than in terrestrial and arboreal forms, which were found to have more subtle differentiation and fewer endemics. Scansorial species could not be set apart from terrestrial ones in terms of appendicular morphology, suggesting that these two modes of locomotion are the most similar and generalized for the group, as they occur in most lineages in the subfamily. The results of this study corroborate previous observations on the relevance of appendicular characters in the differentiation of species and genera in the subfamily Sigmodontinae. J. Morphol. 2013. © 2013 Wiley Periodicals, Inc.