Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats

Flapping flight has evolved independently in three vertebrate clades: pterosaurs, birds and bats. Each clade has a unique flight mechanism involving different elements of the forelimb. Here, patterns of limb integration are examined using partial correlation analysis within species and matrix correlation analysis across species to test whether the evolution of flapping flight has involved developmental dissociation of the serial homologues in the fore- and hind limb in each clade. Our sample included seven species of birds, six species of bats, and three species of pterosaurs for which sufficient sample sizes were available. Our results showed that, in contrast to results previously reported for quadrupedal mammals, none of the three clades demonstrated significant integration between serial homologues in the fore- and hind limb. Unexpectedly, there were few consistent patterns of within-forelimb correlations across each clade, suggesting that wing integration is not strongly constrained by functional relationships. However, there was significant integration within the hind limbs of pterosaurs and birds, but not bats, possibly reflecting the differing functions of hind limbs (e.g. upright support vs. suspension) in these clades.     

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.     

Optimal body size with respect to maximal speed for the yellow-spotted monitor lizard (Varanus panoptes; Varanidae)

Studies of locomotor performance often link variation in morphology with ecology. While maximum sprint speed is a commonly used performance variable, the absolute limits for this performance trait are not completely understood. Absolute maximal speed has often been shown to increase linearly with body size, but several comparative studies covering a large range of body sizes suggest that maximal speed does not increase indefinitely with body mass but rather reaches an optimum after which speed declines. Because of the comparative nature of these studies, it is difficult to determine whether this decrease is due to biomechanical constraints on maximal speed or is a consequence of phylogenetic inertia or perhaps relaxed selection for lower maximal speed at large body size. To explore this issue, we have examined intraspecific variations in morphology, maximal sprint speed, and kinematics for the yellow-spotted monitor lizard Varanus panoptes, which varied in body mass from 0.09 to 5.75 kg. We show a curvilinear relationship between body size and absolute maximal sprint speed with an optimal body mass with respect to speed of 1.245 kg. This excludes the phylogenetic inertia hypothesis, because this effect should be absent intraspecifically, while supporting the biomechanical constraints hypothesis. The relaxed selection hypothesis cannot be excluded if there is a size-based behavioral shift intraspecifically, but the biomechanical constraints hypothesis is better supported from kinematic analyses. Kinematic measurements of hind limb movement suggest that the distance moved by the body during the stance phase may limit maximum speed. This limit is thought to be imposed by a decreased ability of the bones and muscles to support body mass for larger lizards.     

Does metatarsal/femur ratio predict maximal running speed in cursorial mammals?

We tested the hypothesis that hind limb proportions may be used to predict locomotor performance in a sample of 49 species of primarily cursorial mamals. Data on maximal sprint running speeds taken from published sources were related to measurements of hind limb lengths. To control for statistical complications due to the hierarchical nature of phylogenetic relationships, we used Felsenstein's (1985) independent contrasts method for analysing comparative data, and a composite phylogeny for all 49 species, based on a variety of published sources. The independent contrasts method indicates that maximal running speed does not covary significantly with body mass for this sample of mammals (mass range= 2.5–2,000 kg). Even though quality of the available speed data is highly variable, both metatarsal/femur ratio—the traditional index of 'cursoriality' in mammals—and hind limb length (corrected for body size) are significant predictors of maximal running speed. When only fully curorial species are included in the analyses (n = 32), hind limb length still significantly predicts speed (r²= 16%), but MT/F ratio does not. Although ungulates tend to have larger MT/F ratios than do Carnivora, they are not generally faster; relatonships between speed and limb proportions within the two clades show no significant differences. These and previous results suggest that hind limb proportions and maximal running speed may not have evolved in a tightly coupled fashion. Prediction of locomotor performance of extinct forms, based solely on their limb proportions, should be undertaken with caution.     

Epigenetic Effects on Integration of Limb Lengths in a Mouse Model: Selective Breeding for High Voluntary Locomotor Activity

Mammals exhibit a similar pattern of integration among homologous limb elements, the strength of which is believed to vary in response to selection for functional coordination or similarity. Although integration is hypothesized to primarily reflect the effect of genes intrinsic to limbs, extrinsic genetic or epigenetic factors may also affect the strength of integration through their impact on the magnitude and direction of skeletal variance or covariance. Such factors as neuromuscular coordination or bone-muscle interactions may therefore play a role in both canalization and the structure or magnitude of limb integration. If this were the case, then increased levels of locomotor activity would be predicted to increase canalization and the magnitude of covariation between limbs. To investigate whether postnatal activity levels can have a significant effect on variance within or covariance among homologous limb elements, we compared four groups of male mice from a long-term selective breeding experiment: (1) mice from lines bred for increased voluntary activity on running wheels and allowed free access to a wheel for 8 weeks beginning at weaning (“active”), (2) selected mice that did not have wheel access (“sedentary”), (3) active mice from non-selected control lines, and (4) sedentary control mice. Mice from selected lines that had wheel access ran significantly more than control-line mice. However, when controlled for activity, linetype, and body mass, results indicate few significant differences in means, variance, or covariation structure, and no significant differences in integration between limbs, suggesting that postnatal activity levels do not significantly affect canalization or integration of limb lengths. A possible explanation for this result is that whereas baseline levels of postnatal activity may help to maintain patterns of variance and integration, increased levels of activity do not further increase these measures. Investigations into disrupted epigenetic processes (e.g., via models in which neuromuscular coordination is impaired) are required to further test hypotheses about how canalization or integration of limb variation is affected by epigenetic factors.     

Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion

Most quadrupedal mammals support a larger amount of body weight on their forelimbs compared with their hind limbs during locomotion, whereas most primates support more of their body weight on their hind limbs. Increased hind limb weight support is generally interpreted as an adaptation that reduces stress on primates' highly mobile forelimb joints. Thus, increased hind limb weight support was likely vital for the evolution of primate arboreality. Despite its evolutionary importance, the mechanism used by primates to achieve this important kinetic pattern remains unclear. Here, we examine weight support patterns in a sample of chimpanzees (Pan troglodytes) to test the hypothesis that limb position, combined with whole body center of mass position (COM), explains increased hind limb weight support in this taxon. Chimpanzees have a COM midway between their shoulders and hips and walk with a relatively protracted hind limb and a relatively vertical forelimb, averaged over a step. Thus, the limb kinematics of chimpanzees brings their feet closer to the COM than their hands, generating greater hind limb weight support. Comparative data suggest that these same factors likely explain weight support patterns for a broader sample of primates. It remains unclear whether primates use these limb kinematics to increase hind limb weight support, or whether they are byproducts of other gait characteristics. The latter hypothesis raises the intriguing possibility that primate weight support patterns actually evolved as byproducts of other traits, or spandrels, rather than as adaptations to increase forelimb mobility. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Skeletal indicators of locomotor adaptations in living and extinct rodents

Living rodents show great diversity in their locomotor habits, including semiaquatic, arboreal, fossorial, ricochetal, and gliding species from multiple families. To assess the association between limb morphology and locomotor habits, the appendicular skeletons of 65 rodent genera from 16 families were measured. Ecomorphological analyses of various locomotor types revealed consistent differences in postcranial skeletal morphology that relate to functionally important traits. Behaviorally similar taxa showed convergent morphological characters, despite distinct evolutionary histories. Semiaquatic rodents displayed relatively robust bones, enlarged muscular attachments, short femora, and elongate hind feet. Arboreal rodents had relatively elongate humeri and digits, short olecranon processes of the ulnae, and equally proportioned fore and hind limbs. Fossorial rodents showed relatively robust bones, enlarged muscular attachments, short antebrachii and digits, elongate manual claws, and reduced hind limb elements. Ricochetal rodents displayed relatively proximal insertion of muscles, disproportionate limbs, elongate tibiae, and elongate hind feet. Gliding rodents had relatively elongate and gracile bones, short olecranon processes of the ulnae, and equally proportioned fore and hind limbs. The morphological differences observed here can readily be used to discriminate extant rodents with different locomotor strategies. This suggests that the method could be applied to extinct rodents, regardless of ancestry, to accurately infer their locomotor ecologies. When applied to an extinct group of rodents, we found two distinct ecomorphs represented in the beaver family (Castoridae), semiaquatic and semifossorial. There was also a progressive trend toward increased body size and increased aquatic specialization in the giant beaver lineage (Castoroidinae). J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Heritabilities of Directional Asymmetry in the Fore- and Hindlimbs of Rabbit Fetuses

Directional asymmetry (DA), where at the population level symmetry differs from zero, has been reported in a wide range of traits and taxa, even for traits in which symmetry is expected to be the target of selection such as limbs or wings. In invertebrates, DA has been suggested to be non-adaptive. In vertebrates, there has been a wealth of research linking morphological asymmetry to behavioural lateralisation. On the other hand, the prenatal expression of DA and evidences for quantitative genetic variation for asymmetry may suggest it is not solely induced by differences in mechanic loading between sides. We estimate quantitative genetic variation of fetal limb asymmetry in a large dataset of rabbits. Our results showed a low but highly significant level of DA that is partially under genetic control for all traits, with forelimbs displaying higher levels of asymmetry. Genetic correlations were positive within limbs, but negative across bones of fore and hind limbs. Environmental correlations were positive for all, but smaller across fore and hind limbs. We discuss our results in light of the existence and maintenance of DA in locomotory traits.     

Sexual size dimorphism in Darevskia raddei (Sauria: Lacertidae) from northwestern Iran

We examined sexual size dimorphism of the rock-dwelling lizard Darevskia raddei (Boettger, 1892) with the help of 30 specimens that were provided from various sources. Eleven metric and seven meristic features were examined. Seven characters (gulars, length of basal tail, femoral pores, length of head, width of head, length of fore limb and length of hind limb) were identified as dimorphic between the two sexes. Some of these characters have important roles in copulation for males, especially the hind limb and the tail base. The number of femoral pores is important in the release of signal components because females release these components to attract males during the mating season. The length of the hind limb as locomotor performance plays an important role during mating, so that the male can grasp the female and adopt the correct position during copulation.     

Does skeletal anatomy reflect adaptation to locomotor patterns? cortical and trabecular architecture in human and nonhuman anthropoids

Although the correspondence between habitual activity and diaphyseal cortical bone morphology has been demonstrated for the fore- and hind-limb long bones of primates, the relationship between trabecular bone architecture and locomotor behavior is less certain. If sub-articular trabecular and diaphyseal cortical bone morphology reflects locomotor patterns, this correspondence would be a valuable tool with which to interpret morphological variation in the skeletal and fossil record. To assess this relationship, high-resolution computed tomography images from both the humeral and femoral head and midshaft of 112 individuals from eight anthropoid genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, and Symphalangus) were analyzed. Within-bone (sub-articular trabeculae vs. mid-diaphysis), between-bone (forelimb vs. hind limb), and among-taxa relative distributions (femoral:humeral) were compared. Three conclusions are evident: (1) Correlations exists between humeral head sub-articular trabecular bone architecture and mid-humerus diaphyseal bone properties; this was not the case in the femur. (2) In contrast to comparisons of inter-limb diaphyseal bone robusticity, among all species femoral head trabecular bone architecture is significantly more substantial (i.e., higher values for mechanically relevant trabecular bone architectural features) than humeral head trabecular bone architecture. (3) Interspecific comparisons of femoral morphology relative to humeral morphology reveal an osteological "locomotor signal" indicative of differential use of the forelimb and hind limb within mid-diaphysis cortical bone geometry, but not within sub-articular trabecular bone architecture.     

Sifaka positional behavior: ontogenetic and quantitative genetic approaches

In many primate species, hands and feet are large relative to neonatal body weight, and they subsequently exhibit negative allometric growth during ontogeny. Here, data are presented showing that this pattern holds for a wild population of lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). Using morphometric data collected on this population, it is shown that younger animals possess relatively large hands and feet. This ontogenetic pattern suggests a simple behavioral test: do juvenile animals with their larger, almost adult‐sized hands and feet locomote on similarly sized substrates as adult animals? Using locomotor bout sampling, this question was tested by collecting positional behavior data on this population. Results from this test find no differences in locomotor behaviors or substrate use between yearlings and adult animals. To place these results in a broader evolutionary context, heritabilities and selection gradients of hands, feet, and other limb elements for animals in this population were estimated. Among limb elements, heritabilities range from 0.16–0.44, with the foot having the lowest value. Positive directional selection acts most strongly on the foot (directional selection gradient = 0.119). The low heritability and positive selection coefficient indicate that selection has acted, and continues to act, on foot size in young animals. These results are interpreted within a functional context with respect to the development of locomotor coordination: larger feet enable young animals to use “adult‐sized” substrates when they move through their habitat. It is suggested that the widespread pattern of negative allometry of the extremities in sifaka and other primates is maintained by selection, and does not simply reflect a primitive developmental pathway that has no adaptive basis. Am J Phys Anthropol 131:261–271, 2006. © 2006 Wiley‐Liss, Inc.     

Locomotor anatomy and biomechanics of the Dmanisi hominins

The Dmanisi hominins inhabited a northern temperate habitat in the southern Caucasus, approximately 1.8 million years ago. This is the oldest population of hominins known outside of Africa. Understanding the set of anatomical and behavioral traits that equipped this population to exploit their seasonal habitat successfully may shed light on the selection pressures shaping early members of the genus Homo and the ecological strategies that permitted the expansion of their range outside of the African subtropics. The abundant stone tools at the site, as well as taphonomic evidence for butchery, suggest that the Dmanisi hominins were active hunters or scavengers. In this study, we examine the locomotor mechanics of the Dmanisi hind limb to test the hypothesis that the inclusion of meat in the diet is associated with an increase in walking and running economy and endurance. Using comparative data from modern humans, chimpanzees, and gorillas, as well as other fossil hominins, we show that the Dmanisi hind limb was functionally similar to modern humans, with a longitudinal plantar arch, increased limb length, and human-like ankle morphology. Other aspects of the foot, specifically metatarsal morphology and tibial torsion, are less derived and similar to earlier hominins. These results are consistent with hypotheses linking hunting and scavenging to improved walking and running performance in early Homo. Primitive retentions in the Dmanisi foot suggest that locomotor evolution continued through the early Pleistocene.     

Relaxed pollinator-mediated selection weakens floral integration in self-compatible taxa of Leavenworthia (Brassicaceae)

Natural selection should favor the integration of floral traits that enhance pollen export and import in plant populations that rely upon pollinators. If this is true, then phenotypic correlations between floral traits should weaken in self-fertilizing groups that do not require pollinator visitation to produce seed. We tested this hypothesis in Leavenworthia, a plant genus in which there have been multiple independent losses of the sporophytic self-incompatibility system found throughout the Brassicaceae. In particular, we conducted phylogenetically independent contrasts of floral trait correlations between two pairs of self-incompatible (SI) and self-compatible (SC) sister taxa. In support of the hypothesis that pollinator-mediated selection integrates floral traits, we found that both SC Leavenworthia taxa have weaker overall floral correlations in comparison to sister taxa that rely upon pollinators. The two independently derived SC Leavenworthia flowers have significantly weaker stamen-petal or pistil-petal correlations, respectively, whereas the stamen-pistil correlation remains constant. These patterns suggest that relaxation of pollinator-mediated selection weakens the integration of traits associated with pollen export and import. The retention of high stamen-pistil correlations in the SC taxa of Leavenworthia further implies that the integration of these traits is either constrained or maintained by selection favoring the successful transfer of pollen within flowers to secure self-pollination.     

Ontogeny of limb force distribution in squirrel monkeys (Saimiri boliviensis): insights into the mechanical bases of primate hind limb dominance

The distribution of peak vertical forces between the forelimbs and the hind limbs is one of the key traits distinguishing primate quadrupedal locomotion from that of other mammals. Whereas most mammals generate greater peak vertical forelimb forces, primates generate greater peak vertical hind limb forces. At the ultimate level, hind limb dominance in limb force distribution is typically interpreted as an adaptation to facilitate fine-branch arboreality. However, the proximate biomechanical bases for primate limb force distribution remain controversial. Three models have been previously proposed. The Center of Mass (COM) Position model attributes primates’ unique mode of limb loading to differences in the position of the whole-body COM relative to the hands and feet. The Active Weight Shift model asserts that primates actively redistribute body weight to their hind limbs by pitching the trunk up via the activation of hind limb retractor muscles. Finally, the Limb Compliance model argues that primates selectively mitigate forelimb forces by maintaining a compliant forelimb and a flat shoulder trajectory. Here, a detailed dataset of ontogenetic changes in morphology and locomotor mechanics in Bolivian squirrel monkeys (Saimiri boliviensis) was employed as a model system to evaluate each of these proposed models in turn. Over the first 10 months of life, squirrel monkeys transitioned from forelimb dominant infants to hind limb dominant juveniles, a change that was precipitated by decreases in peak vertical forelimb forces and increases in peak vertical hind limb forces. Results provided some support for all three of the models, although the COM Position and Active Weight Shift models were most strongly supported by the data. Overall, this study suggests that primates may use a variety of biomechanical strategies to achieve hind limb dominance in limb force distribution.     

Sexual dimorphism in traits related to locomotion: ontogenetic patterns of variation in Podarcis wall lizards

Sexual dimorphism in body size and shape in animals is normally linked to sexual selection mechanisms that modify the morphological properties of each sex. However, sexual dimorphism of ecologically relevant traits may be amplified by natural selection and result in the ecological segregation of both sexes. In the present study, we investigated patterns of sexual dimorphism of morphological traits relevant for locomotion in two lacertid lizards, Podarcis bocagei and Podarcis carbonelli, aiming to identify ontogenetic sources of variation. We analysed trunk and limb variation in relation to total body size, as well as the covariation of different traits, aiming to shed light on the proximate causation of adult sexual dimorphism. We find that, although immatures are generally monomorphic, adult females have a longer trunk, and adult males have longer fore and hind limbs. Both sexes differ substantially with respect to their growth trajectories and relationships between traits, whereas, in some cases, there are signs of morphological constraints delimiting the observed patterns. Because of the direct connection between limb size/shape and locomotor performance, which is relevant both for habitat use and escape from predators, the observed patterns of sexual dimorphism are expected to translate into ecological differences between both sexes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 530–543.     

Morphological variation does not influence locomotor performance within a cohort of hatchling lizards (Amphibolurus muricatus, Agamidae)

A causal link between morphology and performance is a central tenet of ecomorphological analyses, but there are few detailed analyses of exactly how morphological variation within a hatchling cohort maps onto locomotor performance, and especially whether or not different tasks favour different morphologies (or vice versa). We measured morphological traits (including body length, mass, head size, limb proportions and fluctuating asymmetry [FA]) on a large sample of laboratory-incubated hatchling lizards ( Amphibolurus muricatus , Agamidae), and used principal component analysis to reduce this data set to four major axes of variation (size, shape and two FA axes). Running speeds of each lizard were measured on raceways at four inclines, from level (0°) through to steep (45°). Unsurprisingly, steeper inclines reduced locomotor speeds. Absolute body size was the only morphological trait that was consistently related to sprinting performance, and the relationships were similar at each incline. Within-cohort variation in body shape and FA among this large sample was unrelated to locomotor speeds, thus challenging the common assumption of a causal link between these variables. The only exception was a weak trend for greater hind limb length to enhance locomotor performance more at steep inclines than at shallower angles. In general, our data suggest that different morphological traits do not differentially maximize locomotor performance up variable inclines. Overall, our data provide a cautionary note about the generality of causal connections between within-cohort morphological variation and locomotor performance under different environmental contexts.     

International Commission for Protection against Environmental Mutagens and Carcinogens. ICPEMC working paper 5/5. Perspectives in mutation epidemiology. 5. Modern medical practice versus environmental mutagens: their possible dysgenic impact

We do not know how many mutations are being produced in human populations by exposure to environmental mutagens. If these mutagens caused a persistent rise in mutation rates, then ultimately there would be a proportional increase in the frequency of a variety of genetic diseases, including those that are difficult to treat and that require life-long care of affected individuals. In contrast, modern medical practices are relaxing selection pressure selectively with respect to disease, leading to a gradual increase in the frequency of certain genetic and partly genetic diseases that can be effectively treated. The pattern of this increase would differ from condition to condition, depending upon the mode of inheritance and the extent to which selection is relaxed; except for some special cases, the anticipated increase would generally be slow. Additional economic burdens on future society and families imposed by relaxed selection would mainly involve expenditures for relatively inexpensive treatments, and not those for expensive life-long care. Moreover, individuals treated successfully can be expected to contribute productively to society. With education and counseling for those who survive serious dominant and X-linked disorders, and with the development of accurate, inexpensive prenatal diagnosis, the presumed dysgenic effects of relaxed selection could be balanced.     

The functional morphology of weight bearing: limb joint surface area allometry in anthropoid primates

Biomechanical scaling of long bone joint surface areas was investigated in 13 species of anthropoid primates. It was proposed that joint surface areas should scale with positive allometry with respect to body size in order to maintain relatively constant safety factors for joints in small and large animals and that modifications from the overall pattern of scaling may be expected in the limb joints of species exhibiting specialized locomotor behaviours that radically alter limb loading. Within anthropoids, the brachiating primates, white-handed gibbons ( Hylobates lar ) and black-handed spider monkeys ( Ateles geoffroyi ), were used to test this hypothesis. Total joint surface areas were found to scale with significant positive allometry in 11 of 12 limb joints. The observed pattern of interspecific allometry supports the hypothesis that weight bearing is a major constraint on the design of joints. This positive interspecific allometry is reflected at the intraspecific level as well, with larger joints of larger species showing significant intraspecific scaling. Suspensory species showed no significant deviations from the overall anthropoid pattern, despite their reduced compressive loading of the limb joints, even after controlling for joint mobility. These results suggest that, while evolutionary changes in locomotor behaviour that produce significant increases in loading of a joint may be accompanied by selection for increased joint surface areas, adoption of locomotor repertoires that reduce limb loading may have no selective effect on joint morphology, and joint design in these cases will reflect the biomechanics of the ancestral locomotor condition.     

Evolution of chameleon locomotion,or how to become arboreal as a reptile

High-speed, biplanar X-ray motion analysis, X-ray reconstruction of moving morphology (XROMM) and morphological studies have led to the identification of those traits which are considered to be crucial for the evolution of arboreal locomotion in chameleons. The loss of the extensive lateral undulation typical of reptiles needs to be compensated by high mobility in the shoulder girdle and a clear functional regionalization of the trunk. Large limb excursion angles provide a compliant gait and are made possible by a functional parasagittalization of fore- and hind limbs, at least temporarily. All these evolutionary novelties parallel very similar modifications in the evolution of the locomotor apparatus in therian mammals. We propose that the convergent “invention” of dynamic stability and a compliant gait seem to be responsible for the locomotor similarities between chameleons and mammals.