Testing the Role of Cursorial Specializations as Adaptive Key Innovations in Paleocene-Eocene Ungulates of North America

Episodes of rapid faunal turnover in the fossil record are often used to examine processes driving macroevolutionary changes, such as competitive exclusion. The sudden appearance in the earliest Eocene of North America of artiodactyls and perissodactyls, and subsequent decline of endemic “condylarths” constitutes such an episode. It has been suggested that the specializations for high speed locomotion (cursoriality) that are present in artiodactyls and perissodactyls were key innovations of these orders accounting for their success in the Eocene and onwards. A quantitative geometric morphometric analysis of distal femoral articular morphology was used to examine changes in locomotor specializations in North American ungulates across the Paleocene-Eocene boundary. “Condylarths” were found to have displayed a broad range of locomotor adaptions, including cursoriality. The early Eocene had the broadest disparity in terms of taxonomic and locomotor contributions to morphological diversity. Changes in locomotor variety were associated with the disappearance of arboreal taxa, primarily “condylarths.” The initial impact of artiodactyls and perissodactyls in North America on existing locomotor diversity was limited and does not support a competitive exclusion hypothesis.     

Morphology and locomotor adaptations of the bovid femur in relation to habitat

Extant bovids inhabit a wide diversity of environments that range from forest to savanna and display locomotor patterns that are habitat specific. I report here on an investigation of the linkage between these locomotor patterns and habitat based on a study of the morphology of the bovid femur. Femoral head shape, shaft dimensions, and knee structure are examined and support a statistically significant separation of the different morphological complexes present in bovids from forest, broken cover, and savanna habitats. Morphological differences are primarily related to locomotor patterns as reflected in the degree of cursoriality displayed by bovids in different habitats. Cursorial bovids from savanna environments have laterally expanded femoral heads that act to limit the degree of abduction and axial rotation at the hip, and elliptically shaped distal femora that increase the moment arm of the extensor muscles that cross the knee. Forest bovids have spherically shaped femoral heads. This morphology permits a much higher degree of abduction and axial rotation at the hip and appears to provide greater maneuverability in a vegetationally complex habitat. Bovids living in broken cover environments that fall between the extremes of closed canopy forest and savanna display an intermediate set of femoral characters. This approach to the relationship between habitat and locomotion offers a potentially powerful means with which to examine the interplay between structural form and function in bovid evolution.     

Evolution of hindlimb bone dimensions and muscle masses in house mice selectively bred for high voluntary wheel‐running behavior

We have used selective breeding with house mice to study coadaptation of morphology and physiology with the evolution of high daily levels of voluntary exercise. Here, we compared hindlimb bones and muscle masses from the 11th generation of four replicate High Runner (HR) lines of house mice bred for high levels of voluntary wheel running with four non‐selected control (C) lines. Mass, length, diameter, and depth of the femur, tibia‐fibula, and metatarsal bones, as well as masses of gastrocnemius and quadriceps muscles, were compared by analysis of covariance with body mass or body length as the covariate. Mice from HR lines had relatively wider distal femora and deeper proximal tibiae, suggesting larger knee surface areas, and larger femoral heads. Sex differences in bone dimensions were also evident, with males having thicker and shorter hindlimb bones when compared with females. Several interactions between sex, linetype, and/or body mass were observed, and analyses split by sex revealed several cases of sex‐specific responses to selection. A subset of the HR mice in two of the four HR lines expressed the mini‐muscle phenotype, characterized mainly by an ～50% reduction in hindlimb muscle mass, caused by a Mendelian recessive mutation, and known to have been under positive selection in the HR lines. Mini‐muscle individuals had elongated distal elements, lighter and thinner hindlimb bones, altered 3rd trochanter muscle insertion positions, and thicker tibia‐fibula distal widths. Finally, several differences in levels of directional or fluctuating asymmetry in bone dimensions were observed between HR and C, mini‐ and normal‐muscled mice, and the sexes. This study demonstrates that skeletal dimensions and muscle masses can evolve rapidly in response to directional selection on locomotor behavior.     

Locomotion in some small to medium-sized mammals: a geometric morphometric analysis of the penultimate lumbar vertebra,pelvis and hindlimbs

We assessed the influence of a variety of aspects of locomotion and ecology including gait and locomotor types, maximal running speed, home range, and body size on postcranial shape variation in small to medium-sized mammals, employing geometric morphometric analysis and phylogenetic comparative methods. The four views analyzed, i.e., dorsal view of the penultimate lumbar vertebra, lateral view of the pelvis, posterior view of the proximal femur and proximal view of the tibia, showed clear phylogenetic signal and interesting patterns of association with movement. Variation in home range size was related to some tibia shape changes, while speed was associated with lumbar vertebra, pelvis and tibia shape changes. Femur shape was not related to any locomotor variables. In both locomotor type and high-speed gait analyses, locomotor groups were distinguished in both pelvis and tibia shape analyses. These results suggest that adaptations to both typical and high-speed gaits could explain a considerable portion of the shape of those elements. In addition, lumbar vertebra and tibia showed non-significant relationships with body mass, which suggests that they might be used in morpho-functional analyses and locomotor inferences on fossil taxa, with little or no bias for body size. Lastly, we observed morpho-functional convergences among several mammalian taxa and detected some taxa that achieve similar locomotor features following different morphological paths.     

Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice

Studies of rodents have shown that both forced and voluntary chronic exercise cause increased hindlimb bone diameter, mass, and strength. Among species of mammals, "cursoriality" is generally associated with longer limbs as well as relative lengthening of distal limb segments, resulting in an increased metatarsal/femur (MT/F) ratio. Indeed, we show that phylogenetic analyses of previously published data indicate a positive correlation between body mass-corrected home range area and both hindlimb length and MT/F in a sample of 19 species of Carnivora, although only the former is statistically significant in a multiple regression. Therefore, we used an experimental evolution approach to test for possible adaptive changes (in response to selective breeding and/or chronic exercise) in hindlimb bones of four replicate lines of house mice bred for high voluntary wheel running (S lines) for 21 generations and in four nonselected control (C) lines. We examined femur, tibiafibula, and longest metatarsal of males housed either with or without wheel access for 2 months beginning at 25-28 days of age. As expected from previous studies, mice from S lines ran more than C (primarily because the former ran faster) and were smaller in body size (both mass and length). Wheel access reduced body mass (but not length) of both S and C mice. Analysis of covariance (ANCOVA) revealed that body mass was a statistically significant predictor of all bone measures except MT/F ratio; therefore, all results reported are from ANCOVAs. Bone lengths were not significantly affected by either linetype (S vs. C) or wheel access. However, with body mass as a covariate, S mice had significantly thicker femora and tibiafibulae, and wheel access also significantly increased diameters. Mice from S lines also had heavier feet than C, and wheel access increased both foot and tibiafibula mass. Thus, the directions of evolutionary and phenotypic adaptation are generally consistent. Additionally, S-line individuals with the mini-muscle phenotype (homozygous for a Mendelian recessive allele that halves hindlimb muscle mass [Garland et al., 2002, Evolution 56:1,267-1,275]) exhibited significantly longer and thinner femora and tibiafibulae, with no difference in bone masses. Two results were considered surprising. First, no differences were found in the MT/F ratio (the classic indicator of cursoriality). Second, we did not find a significant interaction between linetype and wheel access for any trait, despite the higher running rate of S mice.     

Sexual dimorphism and interpopulation differences in lizard hind limb length: locomotor performance or chemical signalling?

Intraspecific variation in morphology has often been related to fitness differences through its effects on performance. In lizards, variation in hind limb length can be shaped by natural selection for increased locomotor performance, sexual selection on the number or size of femoral pores involved in chemical signalling, or both. Here, we analyse the selective forces involved in sexual dimorphism and differences in hind limb length between two populations of Psammodromus algirus living at different elevation. Males were more robust and had longer hind limbs and limb segments than females, and low‐elevation lizards had longer limbs than high‐elevation lizards. However, differences in locomotor performance were small and non‐significant, making natural selection for faster runs an unlikely explanation for the observed pattern. On the other hand, males had more femoral pores than females, and lizards had more pores at lower elevation, although the difference was significant only for males (which invest more in chemical signalling). In males, the number of pores, which remains constant along a lizard's life, was not correlated with hind limb length. However, femur length was positively correlated with mean pore size, allowing low‐elevation males to have larger than expected pores, which could increase the effectiveness with which they spread their signals in a dry and warm habitat where chemicals become volatile rapidly. Also, saturation of the sexual coloration of the head was higher for low‐elevation males, suggesting that sexual selection pressures may be more intense. Overall, our results indicate that sexual selection plays a significant role in shaping intraspecific variation in hind limb length. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 318–329.     

Phenotypic disparity of the elbow joint in domestic dogs and wild carnivores*

In this article, I use geometric morphometrics in 2D from a sample of 366 elbow joints to quantify phenotypic disparity in domestic dog breeds, in wild canids, and across the order Carnivora. The elbow joint is a well‐established morphological indicator of forearm motion and, by extension, of functional adaptations toward locomotor or predatory behavior in living carnivores. The study of the elbow joint in domestic dogs allows the exploration of potential convergences between (i) pursuit predators and fast‐running dogs, and (ii) ambush predators and fighting breeds. The results indicate that elbow shape disparity among domestic dogs exceeds than in wolves; it is comparable to the disparity of wild Caninae, but is significantly lower than the one observed throughout Canidae and Carnivora. Moreover, fast‐running and fighting breeds are not convergent in elbow joint shape with extreme pursuit and ambush wild carnivores, respectively. The role of artificial selection and developmental constraints in shaping limb phenotypic disparity through the extremely fast evolution of the domestic dog is discussed in the light of this new evidence.     

Sprint speed is not reduced by exaggerated male weapons in a flower beetle Dicronocephalus wallichii

Exaggerated sexually selected traits are assumed to decrease the mobility of bearers. However, previous empirical studies have often failed to support this assumption, possibly because locomotor performance represents the integration of numerous morphological, physiological and behavioural traits. Males of a flower beetle Dicronocephalus wallichii Pouillaude 1914 (Coleoptera: Scarabaeidae: Cetoniinae) possess elongated forelegs and a pair of exaggerated horns, which are used as dual weapons in male–male competition for mates. We investigated whether these two sexual traits impede the maximum sprint speed on bamboo branches with different angles and thicknesses under laboratory conditions. Our results suggested that no negative relationship exists between relative foreleg length or horn length and sprint speed. Elongated forelegs and horns may entail negligible locomotor costs. Males with longer horns and forelegs were found to have longer midlegs and hindlegs independent of body size. Thus, elongated midlegs and hindlegs in males may enhance balance, stabilize running on bamboo branches and compensate for the locomotor costs of bearing exaggerated weapons. Furthermore, a positive relationship was found between horn length and sprint speed on a horizontal branch. Males with longer horns probably have more energy and/or invest more heavily in appendage musculature. As is known in other animals, male horns of D. wallichii may act as honest indicators of body condition.     

The relative importance of genetics and phenotypic plasticity in dictating bone morphology and mechanics in aged mice: evidence from an artificial selection experiment

Both genetic and environmental factors are known to influence the structure of bone, contributing to its mechanical behavior during, and adaptive response to, loading. We introduce a novel approach to simultaneously address the genetically mediated, exercise-related effects on bone morphometrics and strength, using mice that had been selectively bred for high levels of voluntary wheel running (16 generations). Female mice from high running and control lines were either allowed (n=12, 12, respectively) or denied (n=11, 12, respectively) access to wheels for 20 months. Femoral shaft, neck, and head were measured with calipers and via micro-computed tomography. Fracture characteristics of the femoral head were assessed in cantilever bending. After adjusting for variation in body mass by two-way analysis of covariance, distal width of the femur increased as a result of selective breeding, and mediolateral femoral diameter was reduced by wheel access. Cross-sectional area of the femoral mid-shaft showed a significant linetype x activity effect, increasing with wheel access in high-running lines but decreasing in control lines. Body mass was significantly positively correlated with many of the morphometric traits studied. Fracture load of the femoral neck was strongly positively predicted by morphometric traits of the femoral neck (r2>0.30), but no significant effects of selective breeding or wheel access were found. The significant correlations of body mass with femoral morphometric traits underscore the importance of controlling for body size when analyzing the response of bone size and shape to experimental treatments. After controlling for body mass, measures of the femoral neck remain significant predictors of femoral neck strength.     

Assessing astragalar morphology and biomechanics in western Palaearctic Bison populations with geometric morphometrics

Having arrived 1.8 Ma ago, bison prevailed in the bovid assemblages of the European subcontinent for more than 1.5 Ma. The current geometric morphometric study outlines a framework of ecomorphological differences among several Bison populations of the western Palaearctic, shown by inferences from the tibial and tarsal joint surfaces of their astragalus. Given the principal biomechanical role of this element in the locomotion mechanism, its anatomical features could be linked to diverse functional aspects. In terms of morphological affinity, it is possible to attribute the studied fossil Bison astragalar material to several morphological trends. Shape variation is not explained by size differences and is possibly associated with an open-close habitat gradient, as indicated by the presence of expanded or compressed astragali, respectively. This intragroup spatial and temporal phenotypic diversity among the examined populations could indicate a biogeographic segregation influenced by regional climatic and landscape heterogeneity in the European territory during Pleistocene. Furthermore, a relation to habitat-specific locomotor ecology could be supported, revealing forms with increased cursoriality, operating in open biomes and closed-country dwellers as well.     

Scaling of cursoriality in mammals

Data on limb bone lengths from 64 mammalian species were combined with data on 114 bovid species (Scott, '79) to assess the scaling of limb lengths and proportions in mammals ranging from 0.002 to 364 kg. We analyzed log-transformed data using both reduced major axis and least-squares regression to focus on the distribution across mammals of two key traits—limb length and metatarsal/femur ratio—associated with cursorial adaptation. The total lengths of both fore and hindlimbs scale in a manner very close to the M^0.33 predicted by geometric similarity. Thus the relative limb lengths of large mammals, including bovids, generally regarded among the most cursorial of mammals, are very similar to those of the rodents and insectivores in this sample. Metatarsal/femur ratio also shows little change with changing mass, although bovids tend to have relatively longer metapodials than do other families in the sample. We argue that many of the remaining morphological traits associated with cursoriality (e.g., reduction in joint mobility and number of distal limb bone elements) promote cursoriality only at large body sizes. These results lead us to question the general perception that cursoriality is most widespread among large mammals. We also suggest that discussions of cursoriality should focus explicitly on the two partially independent aspects of performance that are otherwise confounded under this general term—speed and the ability to cover substantial distance. © 1993 Wiley-Liss, Inc.     

Sexual differences in locomotor performance in Tropidurus catalanensis lizards (Squamata: Tropiduridae) – body shape,size and limb musculature explain variation between males and females

Sexual dimorphism (SD) is the evolutionary outcome of selection acting differently on males and females. Several studies describe sexual differences in body size, although other morphological traits might be allometric between sexes and imply functional consequences. Here we test whether morphological differences between sexes in size and shape in the lizard Tropidurus catalanensis explain variation in performance of four locomotor traits. Our results show that males are larger than females and also exhibit longer limbs, longer muscles and larger muscle cross‐sectional areas, while females have longer trunks and more sharped anterior claws; males outperform females in all locomotor performances measured. Sexual differences in sprinting and climbing is related with body size, and climbing performance is also explained by limb lengths, by differences in lengths and cross‐sectional areas of specific muscles, and by interlimb distances. Between‐sex differences in exertion are also related to SD, despite associations with sharper posterior claws that are independent of sex. Grasping performance, however, is associated with some muscle and morphological parameters that are not sexually dimorphic. Together our results suggest that morphology might be under sexual selection in T. catalanensis, given that better locomotor performance likely favours male lizards in typical activities of this polygenic species, such as territory defence and female acquisition. Moreover, the longer trunks that characterize females may confer more space to accommodate eggs. On the other hand, territory defence by males probably increases their exposure to predators, resulting in a synergistic effect of sexual and natural selection in the evolution of SD in T. catalanensis.     

Brief communication: Paleobiological inferences on the locomotor repertoire of extinct hominoids based on femoral neck cortical thickness: The fossil great ape hispanopithecus laietanus as a test-case study

The relationship between femoral neck superior and inferior cortical thickness in primates is related to locomotor behavior. This relationship has been employed to infer bipedalism in fossil hominins, although bipeds share the same pattern of generalized quadrupeds, where the superior cortex is thinner than the inferior one. In contrast, knuckle‐walkers and specialized suspensory taxa display a more homogeneous distribution of cortical bone. These different patterns, probably related to the range of movement at the hip joint and concomitant differences in the load stresses at the femoral neck, are very promising for making locomotor inferences in extinct primates. To evaluate the utility of this feature in the fossil record, we relied on computed tomography applied to the femur of the Late Miocene hominoid Hispanopithecus laietanus as a test‐case study. Both an orthograde body plan and orang‐like suspensory adaptations had been previously documented for this taxon on different anatomical grounds, leading to the hypothesis that this fossil ape should display a modern ape‐like distribution of femoral neck cortical thickness. This is confirmed by the results of this study, leading to the conclusion that Hispanopithecus represents the oldest evidence of a homogeneous cortical bone distribution in the hominoid fossil record. Our results therefore strengthen the utility of femoral neck cortical thickness for making paleobiological inferences on the locomotor repertoire of fossil primates. This feature would be particularly useful for assessing the degree of orthograde arboreal locomotor behaviors vs. terrestrial bipedalism in putative early hominins. Am J PhyAnthropol 2012. © Wiley Periodicals, Inc.     

Prey processing in Leurognathus marmoratus and the evolution of form, and function in desmognathine salamanders (Plethodontidae)

Function and biological role of morphological specialization in desmognathine salamanders are analysed in the light of studies of feeding in Leurognatthus marmoratus. Nine morphological features uniquely characterize the Desmognathinae as compared to its sister group, the Plethodontinae, and other salamanders: (1) heavily ossified and strongly articulated skull and mandible; (2) flat, wedgelike head profile; (3) stalked occipital condyles; (4) modified atlas; (5) modified anterior trunk vertebrae; (6) atlanto-mandibular ligaments; (7) enlarged dorsal spinal muscles; (8) enlarged quadrato-pectoralis muscles; and (9) hind limbs relatively larger than forelimbs. Dorsoventral head mobility is increased at the atlanto-occipital joint by the stalked occipital condyles which simultaneously increase the mechanical advantage of the hypertrophied axial muscles that cross the joint. During head depression the atlanto-mandibular ligaments are placed in tension. Force generated by the quadrato-pectoralis muscles is transmitted directly to the mandible, creating a powerful bite with the jaws in full occlusion. Desmognathines use an efficient static pressure system for subduing and/or killing prey items held in the jaws, not a kinetic-inertial mechanism, as previously suggested. Leurognathus exhibits a behaviour ('head-tucking') unique to desmognathines that is consistent with the static-pressure hypothesis. Several desmognathine features (1, 2, 5, 7, 9) are not explicable as adaptations for feeding; these function as locomotory specializations for burrowing, especially for wedging under rocks within and alongside streams. Desmognathines use head-tucking during such wedging and burrowing movements, thus locomotory specializations act in concert with the feeding specializations. We suggest that origin of the atlanto-mandibular ligaments can be considered a 'key innovation' in that it allowed the secondary invasion of stream habitats by adults of ancestral desmognathines.     

Genomic signatures of diet-related shifts during human origins

There are numerous anthropological analyses concerning the importance of diet during human evolution. Diet is thought to have had a profound influence on the human phenotype, and dietary differences have been hypothesized to contribute to the dramatic morphological changes seen in modern humans as compared with non-human primates. Here, we attempt to integrate the results of new genomic studies within this well-developed anthropological context. We then review the current evidence for adaptation related to diet, both at the level of sequence changes and gene expression. Finally, we propose some ways in which new technologies can help identify specific genomic adaptations that have resulted in metabolic and morphological differences between humans and non-human primates.     

The functional anatomy of the forelimb of some African viverridae (Carnivora)

The functional morphology of the forelimbs of the following African Viverridae was studied, Atilax paludinosus, Bdeogale crassicauda, Civettictis civetta, Genetta genetta, G. tigrina, Helogale parvula, Herpestes ichneumon, H. sanguineus, Ichneumia albicauda, Mungos mungo, Nandinia binotata. Their locomotory behaviour has been previously studied and described and is related to morphological differences. The osteology of all the species and the myology of three species is described. The species have been assigned to primary locomotor categories on the basis of their locomotion. These are 1, climbing, arboreal walking; 2, arboreal and terrestrial walking and jumping; 3, general terrestrial walking and scrambling; and 4, trotting. In the climbing arboreal walking category the most distinctive morphological adaptations are powerful flexors and extensors as well as a flexible plantigrade manus with retractile claws. In the arboreal and terrestrial walking category the shoulder, elbow and carpal joints are flexible and the manus has retractile claws, though the flexor and extensor musculature is insufficiently developed for controlled climbing. The trotting category is characterised by a high humero-radial index and a rigid antibrachium. The foot is digitigrade with the claws short and stout. Species in the general walking and scrambling category show many differences in the morphology of their feet, even though the proximal parts of the forelimb appear similar. Due to the restricted nature of the adaptations, these species have been assigned to secondary locomotor categories. Morphological characters typical of the locomotor categories are summarized in the discussion.     

The functional anatomy of the hindlimb of some African Viverridae (Carnivora).

The functional anatomy of the hindlimb of 12 species of viverrids was studied with relation to locomotion. The animals were allocated to primary locomotor categories on the basis of their anatomy and locomotion. The climbing, arboreal walking category (Nandinia binotata) is characterized by a small sacroiliac articulation, the iliopsoas inserts onto a medially located lesser trochanter and the femoral condyles are not posteriorly placed. The hindfoot is plantigrade and its structure permits considerable movement. The pads are soft and the claws retractile. Representatives of the arboreal and terrestrial walking and jumping category (Genetta genetta, G. servalina, G. tigrina) have a plantigrade forefoot and digitigrade hindfoot. The lesser trochanter is more posteriorly placed than in the climbing category. A previously undescribed muscle, the caudofemoralis profundus extends from several anterior caudal vertebrae to the femur. The tibio-astragular joint restricts supination of the foot. There is little mediolateral movement in the digitidgrade foot. The claws are retractile. In the general terrestrial walking and scrambling group (Helogale parvula, Mungos mungo, Atilax paludinosus, Bdeogale crassicauda, Herpestes ichneumon, H. sanguineus) the animals have essentially similar hindlimbs except for size differences and modifications to the feet. Helogale and Mungos have large medial epicondyles on the humerus and large terminal phalanges. Bdeogale has a vestigial first metatarsal, while Atilax can splay its digits. In all species the distal phalanges are non-retractile. The trotting category (Civettictis civetta, Ichneumia albicauda) is characterized by longer epipodials and metapodials and a more proximal position of muscle bellies. Most of the adaptations minimize rotation, adduction and abduction of the leg and supination of the foot. The metatarsals are closely adjoined and the distal phalanx is stout and non-retractile. There appear to be two levels of locomotory adaptation. Major adaptations affect the whole appendicular skeleton and are used to assign animals to primary locomotor categories. Minor adaptations occur mainly in the foot and indicate the more specific habits of the animal.     

Song complexity is associated with habitat quality in an upland passerine

Understanding the influence of intrinsic (genetic and morphological) and extrinsic (geographical, environmental and social) factors on the performance and spatial differentiation of sexual signals, such as bird song, can help identify behavioural indicators of individual quality, habitat degradation and social environment. We used the Iberian Bluethroat Luscinia svecica azuricollis, a migratory bird that breeds in fragmented landscapes dominated by shrublands, as a case study to: (1) assess how a set of acoustic indicators of song performance are driven by intrinsic and extrinsic factors; and (2) contrast deterministic (adaptations to the environmental context and morphological constraints) vs. stochastic (differentiation by geographical isolation) explanations for song differentiation patterns. We explored acoustic indicators of song performance (spectral, temporal and song complexity) in relation to parameters related to genetic structure, body size, habitat type, habitat quality (assessed through a spatially explicit modelling approach) and social context (population abundance and songbird community composition). Then, we explored the contribution of genetic, geographical and environmental dissimilarity to song diversification across space. Our results highlight an association of song spectral variables with genetic structure and a significant connection between song complexity and duration with habitat quality. We found no relationship between social features and acoustic variables, or between song differentiation and genetic or geographical distances. There was, however, a correlation between song differentiation and environmental dissimilarity. We recommend the consideration of song complexity as an indicator of habitat quality.