Article

Early primate evolution: insights into the functional significance of grasping from motion analyses of extant mammals

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Abstract

Despite differences in the assumed ecological context in competing evolutionary scenarios for early primate locomotion, there appears to be consensus about the adaptive significance of grasping for the exploitation of the terminal branch habitat. I attempt to review first the phylogenetic framework of early primate evolution. Then, I focus on proposed extant analogues for potential ancestral morphotypes of early primate evolution and motion analyses conducted to gain insight specifically into the role of grasping during small-branch locomotion. Studies concerned with proposed extant analogues, such as treeshrews, didelphid marsupials, mouse lemurs, tamarins and marmosets, marsupial gliders and various small arboreal rodents, are summarized. This overview demonstrates a striking variability and plasticity of strategies to cope with the challenging functional demands of locomotion in the terminal branch habitat and helps to identify open questions for further research. For example, potential morphological correlates for specific behaviours still need to be validated in future in-depth quantitative experimental studies. Comparative approaches beyond the anatomy that specifically account for data on locomotor and postural behaviour of extant species, also including phylogenetically informed analyses, are mostly lacking and should be intended to link evolutionary patterns of morphological change with functional characteristics observed in experimental studies.

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... Tamarins (belonging to Callitrichidae, within platyrrhine primates), as all other arboreal mammals, are faced with specific functional demands for the locomotor system due to discontinuous, narrow, and flexible supports, which these animals need to be able to navigate to bridge gaps and reach food sources such as fruits, flowers, and invertebrates (see recent review [17]). For example, the movement on thin and flexible (i.e., precipitously bending) terminal branches, where usually the fruit and flowers are located, represents a challenge for the required balance [17][18][19][20][21]. Accordingly, support diameter and support flexibility should be considered as environmental variables that exert significant selective pressure on the locomotor apparatus (e.g., to stabilize the shoulder and elbow on flexible supports [16]) of such arboreal mammals [22,23]. ...
... Tamarins (belonging to Callitrichidae, within platyrrhine primates), as all other arboreal mammals, are faced with specific functional demands for the locomotor system due to discontinuous, narrow, and flexible supports, which these animals need to be able to navigate to bridge gaps and reach food sources such as fruits, flowers, and invertebrates (see recent review [17]). For example, the movement on thin and flexible (i.e., precipitously bending) terminal branches, where usually the fruit and flowers are located, represents a challenge for the required balance [17][18][19][20][21]. Accordingly, support diameter and support flexibility should be considered as environmental variables that exert significant selective pressure on the locomotor apparatus (e.g., to stabilize the shoulder and elbow on flexible supports [16]) of such arboreal mammals [22,23]. ...
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Background Biological adaptation manifests itself at the interface of different biologically relevant ‘levels’, such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these ‘levels’. Results We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons . We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax , based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two. Conclusion This study demonstrates the complex ways in which behavioral and morphological ‘levels’ map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.
... LS gaits are the most commonly observed gaits in quadrupedal mammals (Hildebrand, 1966(Hildebrand, , 1967(Hildebrand, , 1976Cartmill et al., 2002), probably even representing the ancestral state of tetrapods (Wimberly et al., 2021). Diagonal sequences (DS) are displayed in arboreal marsupials Shapiro and Young, 2010;Gaschk et al., 2019;Nyakatura, 2019), primates (Hildebrand, 1967;Nyakatura et al., 2008) and a few examples reported outside these groups (e.g. kinkajou; Lemelin and Cartmill, 2010). ...
... Tamanduas employ LSDC gaits, use their tail when balancing and adjust hand/foot posture Whereas grasping arboreal primates and marsupials predominantly display DSDC gaits (Hildebrand, 1967;Schmitt and Lemelin, 2002;Nyakatura et al., 2008;Lemelin and Cartmill, 2010;Nyakatura, 2019) on (simulated) branches, tamanduas shift from LSLC gaits (D<0.25) on the ground to LSDC gaits (0.25<D<0.5) on branches. LSDC gait sequences on arboreal supports have also been reported for small arboreal species with less specialised grasping adaptations TD TD TD TD TD TD TD TD Stance phase Swing phase Stance phase Swing phase 3 3 3 4 4 5 5 5 5 5 5 5 5 6 5 5 6 6 6 5 5 2 2 2 1 1 0 2 2 3 3 5 6 6 5 5 5 6 5 4 4 2 3 3 4 5 4 5 5 5 5 5 5 5 6 5 6 6 6 6 5 5 2 2 2 1 1 0 2 2 3 4 5 6 6 4 4 3 3 3 2 2 2 3 3 4 5 4 5 5 5 5 5 5 5 6 5 6 6 6 6 5 5 2 2 2 1 1 0 2 2 3 4 5 6 6 4 4 3 3 3 2 2 ...
Article
Therian mammals are known to move their forelimbs in a parasagittal plane, retracting the mobilised scapula during stance phase. Non-cursorial therian mammals often abduct the elbow out of the shoulder-hip parasagittal plane. This is especially prominent in Tamandua (Xenarthra), which suggests they employ aspects of sprawling (e.g., lizard-like-) locomotion. Here, we test if tamanduas use sprawling forelimb kinematics, i.e., a largely immobile scapula with pronounced lateral spine bending and long-axis rotation of the humerus. We analyse high speed videos and use X-ray motion analysis of tamanduas walking and balancing on branches of varying inclinations and provide a quantitative characterization of gaits and forelimb kinematics. Tamanduas displayed lateral sequence lateral-couplets gaits on flat ground and horizontal branches, but increased diagonality on steeper in- and declines, resulting in lateral sequence diagonal-couplets gaits. This result provides further evidence for high diagonality in arboreal species, likely maximising stability in arboreal environments. Further, the results reveal a mosaic of sprawling and parasagittal kinematic characteristics. The abducted elbow results from a constantly internally rotated scapula about its long axis and a retracted humerus. Scapula retraction contributes considerably to stride length. However, lateral rotation in the pectoral region of the spine (range: 21°) is higher than reported for other therian mammals. Instead, it is similar to skinks and alligators, indicating an aspect generally associated with sprawling locomotion is characteristic for forelimb kinematics of tamanduas. Our study contributes to a growing body of evidence of highly variable non-cursorial therian mammal locomotor kinematics.
... Lateral sequence gaits, like DS gaits, are symmetrical gaits, but the hindlimb contact is followed by an ipsilateral forelimb contact. As a proxy for an intermediate stage of primate evolution, marmosets provide an important point of comparison for the current study (Sargis et al., 2007;Nyakatura, 2019). Here, we used squirrel monkeys (Saimiri boliviensis) as a generalized proxy for a fine branch arboreal primate. ...
... A previous study on marmoset locomotion provided insight on how an animal that may resemble an early, nongrasping stage of primate evolution (Nyakatura, 2019) would have to adjust gait kinematics when moving atop precarious branches. Squirrel monkeys, with their enhanced grasping capabilities, model a later fully grasping stage of euprimate evolution (Sargis et al., 2007), and the current study suggests that behavioral changes coincided with better developed grasping morphology (Young & Chadwell, 2020). ...
Article
Arboreal environments require overcoming navigational challenges not typically encountered in other terrestrial habitats. Supports are unevenly distributed and vary in diameter, orientation, and compliance. To better understand the strategies that arboreal animals use to maintain stability in this environment, laboratory researchers must endeavor to mimic those conditions. Here, we evaluate how squirrel monkeys (Saimiri boliviensis) adjust their locomotor mechanics in response to variation in support diameter and compliance. We used high-speed cameras to film two juvenile female monkeys as they walked across poles of varying diameters (5, 2.5, and 1.25 cm). Poles were mounted on either a stiff wooden base ("stable" condition) or foam blocks ("compliant" condition). Six force transducers embedded within the pole trackway recorded substrate reaction forces during locomotion. We predicted that squirrel monkeys would walk more slowly on narrow and compliant supports and adopt more "compliant" gait mechanics, increasing stride lengths, duty factors, and an average number of limbs gripping the support, while the decreasing center of mass height, stride frequencies, and peak forces. We observed few significant adjustments to squirrel monkey locomotor kinematics in response to changes in either support diameter or compliance, and the changes we did observe were often tempered by interactions with locomotor speed. These results differ from a similar study of common marmosets (i.e., Callithrix jacchus, with relatively poor grasping abilities), where variation in diameter and compliance substantially impacted gait kinematics. Squirrel monkeys' strong grasping apparatus, long and mobile tails, and other adaptations for arboreal travel likely facilitate robust locomotor performance despite substrate precarity.
... Similarly to stem placentals, body size of early euarchontans (e.g., plesiadapiforms) was likely small, too (Silcox and López-Torres, 2017). A consensus regarding the phylogenetic affinities of the taxa forming the Euarchontoglires has not been reached despite considerable effort over recent years (reviewed in Nyakatura, 2019). ...
... Considering the likely small body size as suggested by stem placental fossils (Ji et al., 2002;Luo et al., 2011;Youlatos et al., 2015) and early members of the Euarchontoglires (e.g., plesiadapiforms, Silcox and López-Torres, 2017), small body size should be one of the main considerations when identifying potential modern analogs for early primates and further early Euarchontoglires (Nyakatura, 2019). This is especially important considering the size threshold for effective asymmetrical locomotion proposed by Chadwell and Young (2015). ...
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Differences between arboreal and terrestrial supports likely pose less contrasting functional demands on the locomotor system at a small body size. For arboreal mammals of small body size, asymmetrical gaits have been demonstrated to be advantageous to increase dynamic stability. Many of the extant arboreal squirrel-related rodents display a small body size, claws on all digits, and limited prehensility, a combination that was proposed to have characterized the earliest Euarchontoglires. Thus, motion analysis of such a modern analog could shed light onto the early locomotor evolution of eurarchontoglirans. In this study, we investigated how Swinhoe’s striped squirrels (Tamiops swinhoei; Scuiromorpha) adjust their locomotion when faced with different orientations on broad supports and simulated small branches. We simultaneously recorded high-Hz videos (501 trials) and support reaction forces (451 trials) of squirrels running on two types of instrumented trackways installed at either a 45° incline (we recorded locomotion on inclines and declines) or with a horizontal orientation. The striped squirrels almost exclusively used asymmetrical gaits with a preference for full bounds. Locomotion on simulated branches did not differ substantially from locomotion on the flat trackway. We interpreted several of the quantified adjustments on declines and inclines (in comparison to horizontal supports) as mechanisms to increase stability (e.g., by minimizing toppling moments) and as adjustments to the differential loading of fore- and hind limbs on inclined supports. Our data, in addition to published comparative data and similarities to the locomotion of other small arboreal rodents, tree shrews, and primates as well as a likely small body size at the crown-group node of Euarchontoglires, render a preference for asymmetrical gaits in early members of the clade plausible. This contributes to our understanding of the ancestral lifestyle of this mammalian ‘superclade’.
... However, a recent study carried out on the astragalus and calcaneus of the most basal plesiadapiform, Purgatorius, confirms that these animals were arboreal but did not possess a euprimate-like graspleaping behavior (Chester et al., 2015). Instead, they are viewed as arboreal clawed-climbers similar to the living scandentian Ptilocercus lowi, which is also regarded as a good analogue for the ancestral euarchontan (Szalay and Dagosto, 1988;Sargis, 2002Sargis, , 2004Nyakatura, 2019). A remarkable exception is C. simpsoni, whose partial skeleton displays euprimate-like hallucal grasping features (Bloch and Boyer, 2002). ...
Article
The morphological adaptations of euprimates have been linked to their origin and early evolution in an arboreal environment. However, the ancestral and early locomotor repertoire of this group remains contentious. Although some tarsal bones like the astragalus and the calcaneus have been thoroughly studied, the navicular remains poorly studied despite its potential implications for foot mobility. Here, we evaluate early euprimate locomotion by assessing the shape of the navicular—an important component of the midtarsal region of the foot—using three-dimensional geometric morphometrics in relation to quantified locomotor repertoire in a wide data set of extant primates. We also reconstruct the locomotor repertoire of representatives of the major early primate lineages with a novel phylogenetically informed discriminant analysis and characterize the changes that occurred in the navicular during the archaic primate–euprimate transition. To do so, we included in our study an extensive sample of naviculars (36 specimens) belonging to different species of adapiforms, omomyiforms, and plesiadapiforms. Our results indicate that navicular shape embeds a strong functional signal, allowing us to infer the type of locomotion of extinct primates. We demonstrate that early euprimates displayed a diverse locomotor behavior, although they did not reach the level of specialization of some living forms. Finally, we show that the navicular bone experienced substantial reorganization throughout the archaic primate–euprimate transition, supporting the major functional role of the tarsus during early primate evolution. This study demonstrates that navicular shape can be used as a reliable proxy for primate locomotor behavior. In addition, it sheds light on the diverse locomotor behavior of early primates as well as on the archaic primate–euprimate transition, which involved profound morphological changes within the tarsus, including the navicular bone.
... The evolution of prehensility in general has been linked to arboreal habits (Fabre et al., 2013;Sustaita et al., 2013;Nyakatura, 2019) and the idea that prehensile hands are associated with an arboreal lifestyle has been widely accepted since the early 20th century. However, which specific selective pressures drove the development of primate manual prehensility remains an area of debate. ...
Article
Manual grasping is widespread among tetrapods but is more prominent and dexterous in primates. Whether the selective pressures that drove the evolution of dexterous hand grasping involved the collection of fruit or predation on mobile insects remains an area of debate. One way to explore this question is to examine preferences for manual versus oral grasping of a moving object. Previous studies on strepsirrhines have shown a preference for oral-grasping when grasping static food items and a preference for manual-grasping when grasping mobile prey such as insects, but little is known about the factors at play. Using a controlled experiment with a simple and predictable motion of a food item we tested and compared the grasping behaviours of 53 captive individuals belonging to 17 species of strepsirrhines while grasping swinging food items and static food items. The swinging motion increased the frequency of hand-use for all individuals. Our results provide evidence that the swinging motion of the food is a sufficient parameter to increase hand-grasping in a wide variety of strepsirrhine primates. From an evolutionary perspective, this result gives some support to the idea that hand-grasping abilities evolved under selective pressures associated with the predation of food items in motion. Looking at common grasping pattern across a large set of species, this study provides important insight into comparative approaches to understanding the evolution of food hand-grasping in primates and potentially other tetrapod taxa.
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Sensorimotor learning requires reorganization of neuronal activity in the premotor cortex (PM) and primary motor cortex (M1). To reveal PM- and M1-specific reorganization in a primate, we conducted calcium imaging in common marmosets while they learned a two-target reaching (pull/push) task after mastering a one-target reaching (pull) task. Throughout learning of the two-target reaching task, the dorsorostral PM (PMdr) showed peak activity earlier than the dorsocaudal PM (PMdc) and M1. During learning, the reaction time in pull trials increased and correlated strongly with the peak timing of PMdr activity. PMdr showed decreasing representation of newly introduced (push) movement, whereas PMdc and M1 maintained high representation of pull and push movements. Many task-related neurons in PMdc and M1 exhibited a strong preference to either movement direction. PMdc neurons dynamically switched their preferred direction depending on their performance in push trials in the early learning stage, whereas M1 neurons stably retained their preferred direction and high similarity of preferred direction between neighbors. These results suggest that in primate sensorimotor learning, dynamic directional motor tuning in PMdc converts the sensorimotor association formed in PMdr to the stable and specific motor representation of M1.
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Objectives Despite the longstanding importance of grasping adaptations in theories of primate evolution, quantitative data on primate grasping strength remain rare. We present the results of two studies testing the prediction that callitrichines—given their comparative retreat from a small‐branch environment and specialization for movement and foraging on tree trunks and large boughs—should be characterized by weaker grasping forces and underdeveloped digital flexor muscles relative to other platyrrhines. Methods First, we directly measured manual grasping strength in marmosets ( Callithrix jacchus ) and squirrel monkeys ( Saimiri boliviensis ), using a custom‐constructed force transducer. Second, we reanalyzed existing datasets on the fiber architecture of forearm and leg muscles in 12 platyrrhine species, quantifying digital flexor muscle physiological cross‐sectional area (i.e., PCSA, a morphometric proxy of muscle strength) relative to the summed PCSA across all forearm or leg muscles. Results Callithrix was characterized by lower mean and maximum grasping forces than Saimiri , and callitrichines as a clade were found to have relatively underdeveloped manual digital flexor muscle PCSA. However, relative pedal digital flexor PCSA did not significantly differ between callitrichines and other platyrrhines. Conclusions We found partial support for the hypothesis that variation in predominant substrate usage explains variation in empirical measurements of and morphological correlates of grasping strength in platyrrhines. Future research should extend the work presented here by (1) collecting morphological and empirical metrics of grasping strength in additional primate taxa and (2) extending performance testing to include empirical measures of primate pedal grasping forces as well.
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Morphological traits suggesting powerful jumping abilities are characteristic of early crown primate fossils. Because tree squirrels lack certain ‘primatelike’ grasping features but frequently travel on the narrow terminal branches of trees, they make a viable extant model for an early stage of primate evolution. Here, we explore biomechanical determinants of jumping performance in the arboreal Eastern gray squirrel (Sciurus carolinensis, n = 3) as a greater understanding of the biomechanical strategies that squirrels use to modulate jumping performance could inform theories of selection for increased jumping ability during early primate evolution. We assessed vertical jumping performance by using instrumented force platforms upon which were mounted launching supports of various sizes, allowing us to test the influence of substrate diameter on jumping kinetics and performance. We used standard ergometric methods to quantify jumping parameters (e.g., takeoff velocity, total displacement, peak mechanical power) from force platform data during push-off. We found that tree squirrels display divergent mechanical strategies according to the type of substrate, prioritizing force production on flat ground versus center of mass displacement on narrower poles. As jumping represents a significant part of the locomotor behavior of most primates, we suggest that jumping from small arboreal substrates may have acted as a potential driver of the selection for elongated hindlimb segments in primates, allowing the center of mass to be accelerated over a longer distance—and thereby reducing the need for high substrate reaction forces.
Chapter
Arboreal supports impose a set of locomotor challenges not typically encountered in other terrestrial ecosystems. Because all arboreal animals must negotiate this common set of physical challenges in an environment where clumsy mistakes can lead to tragedy (or at least to the increased energetic burden of having to fight gravity to regain a lost position), it is of little surprise that we see widespread convergence of locomotor morphology and behavior among arboreal amphibians, lizards, and mammals. In this chapter I consider the biomechanical challenges imposed by moving on narrow and compliant arboreal supports, and survey existing data on how arboreal amphibians, lizards, and mammals have arrived at morphological and behavioral solutions to these problems. I focus on the biomechanical problems of negotiating narrow and compliant supports given that these challenges are, to some degree, uniquely characteristic of the arboreal environment. Narrow supports potentially compromise locomotor performance in two ways: (1) by increasing the probability that the animal may tangentially slip from the support and, (2) by challenging mediolateral (i.e., transverse/rolling plane) stability. Compliant supports, by contrast, have the potential to reduce locomotor performance by absorbing some of the mechanical energy that the animal could use to accelerate and redirect its center of mass, and then unpredictably returning this energy at random times and in random directions (at least with respect to the animal’s desired movement dynamics). Widespread morphological solutions to the biomechanical problems of moving on narrow and compliant supports include small body size, appendicular joints with enhanced mobility, grasping extremities, and long tails. Convergent behavioral solutions for increasing stability on precarious arboreal supports include reducing speed, increased limb joint flexion, the use of “compliant” gait kinematics marked by elongated limb contact durations (i.e., duty factors), a switch to gaits that facilitate more continuous contact with the substrate (and fewer ballistic aerial phases), and a decrease overall limb stiffness typically accomplished via exaggerated limb joint excursions during the stance phase. Future research on arboreal locomotion in tetrapods should focus on integrating quantitative laboratory data on locomotor kinematics and kinetics with holistic ecological data on substrate use and support morphology gleaned in the field. Such integrated datasets will be critical for furthering our understanding of how locomotor anatomy and behavior are shaped by the rigors of the natural arboreal environment.
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Differential habitat use in sympatric species can provide insight into how behavior relates to morphological differences and as a general model for the study of biological adaptations to different functional demands. In Amazonia, closely related sympatric tamarins of the genera Saguinus and Leontocebus regularly form stable mixed-species groups, but exhibit differences in foraging height and locomotor activity. To test the hypothesis that two closely related species in a mixed-species group prefer different modes of leaping regardless of the substrates available, we quantified leaping behavior in a mixed-species group of Saguinus mystax and Leontocebus nigrifrons. We studied leaping behavior in relation to support substrate type and foraging height in the field for 5 months in the Amazonian forest of north-eastern Peru. Saguinus mystax spent significantly more time above 15 m (79%) and used predominantly horizontal and narrow supports for leaping. Leontocebus nigrifrons was predominantly active below 10 m (87%) and exhibited relatively more trunk-to-trunk leaping. Both species preferred their predominant leaping modes regardless of support type availability in the different forest layers. This indicates that the supports most commonly available in each forest layer do not determine the tamarins’ leaping behavior. This apparent behavioral adaptation provides a baseline for further investigation into how behavioral differences are reflected in the morphology and species-specific biomechanics of leaping behavior and establishes callitrichid primates as a model well-suited to the general study of biological adaptation.
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Locomotion on the narrow and compliant supports of the arboreal environment is inherently precarious. Previous studies have identified a host of morphological and behavioral specializations in arboreal animals broadly thought to promote stability when on precarious substrates. Less well-studied is the role of the tail in maintaining balance. However, prior anatomical studies have found that arboreal taxa frequently have longer tails for their body size than their terrestrial counterparts, and prior laboratory studies of tail kinematics and the effects of tail reduction in focal taxa have broadly supported the hypothesis that the tail is functionally important for maintaining balance on narrow and mobile substrates. In the current set of studies, we extend this work in two ways. First, we use a laboratory dataset on three-dimensional segmental kinematics and tail inertial properties in squirrel monkeys (Saimiri boliviensis) to investigate how tail angular momentum is modulated during steady-state locomotion on narrow supports. In the second study, we use a quantitative dataset on quadrupedal locomotion in wild platyrrhine monkeys to investigate how free-ranging arboreal animals adjust tail movements in response to substrate variation, focusing on kinematic measures validated in prior laboratory studies of tail mechanics (including the laboratory data presented). Our laboratory results show that S. boliviensis significantly increase average tail angular momentum magnitudes and amplitudes on narrow supports, and primarily regulate that momentum by adjusting the linear and angular velocity of the tail (rather than via changes in tail posture per se). We build on these findings in our second study by showing that wild platyrrhines responded to the precarity of narrow and mobile substrates by extending the tail and exaggerating tail displacements, providing ecological validity to the laboratory studies of tail mechanics presented here and elsewhere. In conclusion, our data support the hypothesis that the long and mobile tails of arboreal animals serve a biological role of enhancing stability when moving quadrupedally over narrow and mobile substrates. Tail angular momentum could be used to cancel out the angular momentum generated by other parts of the body during steady-state locomotion, thereby reducing whole-body angular momentum and promoting stability, and could be used to mitigate the effects of destabilizing torques about the support should the animals encounter large, unexpected perturbations. Overall, these studies suggest that long and mobile tails should be considered among the fundamental suite of adaptations promoting safe and efficient arboreal locomotion.
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Fine-branch models have long played a central role in primate evolutionary research. Nevertheless, recent studies of positional behavior in nonprimate arboreal mammals have challenged the idea that synapomorphic primate features, such as grasping extremities, uniquely facilitated access to the fine-branch zone. We test the alternative hypothesis that grasping extremities specifically improve locomotor performance in a fine-branch environment by examining how support diameter influences locomotor mechanics in one sciurid rodent (Sciurus carolinensis) and two platyrrhine primates (Callithrix jacchus and Saimiri boliviensis). These species were chosen to broadly model different stages in the evolution of primate grasping morphology. The results showed that transitioning from broad to narrower supports required the greatest kinematic adjustment in squirrels and the least adjustment in squirrel monkeys, with marmosets displaying an intermediate level of adjustment. Moreover, on any given support, squirrels' locomotor mechanics differed from marmosets' in a manner consistent with a greater need for stability, despite superficial ecomorphological similarities between sciurid rodents and callitrichine primates. Morphological analyses of autopodial size and proportions suggest that variation in locomotor performance more closely tracked variation in overall hand and foot size rather than digit length per se. Indeed, a broad comparative analysis revealed that for their body mass, primates have longer hands than similarly sized arboreal rodents and marsupials (although only the primate-rodent comparison was significant after incorporating phylogenetic relatedness). Inclusion of fossil stem primates (plesiadapiforms) and euprimates (adapiforms) in these analyses suggests that this primate-wide grade shift in relative autopodial size must have occurred early in the evolutionary history of the group. Overall, our findings show that basal primate morphological adaptations may have specifically facilitated improved locomotor performance in a fine-branch niche, rather than merely permitting access to the environment. As such, future adaptive hypotheses of primate origins should incorporate the import of primate-like morphology on locomotor performance as well.
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Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals. Molecular data and the fossil record can give conflicting views of the evolutionary past. For instance, empirical palaeontological evidence by itself tends to favour the 'explosive model' of diversification for extant placental mammals 1 , in which the orders with living representatives both originated and rapidly diversified soon after the Cretaceous/Tertiary (K/T) mass extinction event that eliminated non-avian dinosaurs and many other, mostly marine 2 , taxa 65.5 million years (Myr) ago 1,3,4. By contrast, molecular data consistently push most origins of the same orders back into the Late Cretaceous period 5-9 , leading to alternative scenarios in which placental line-ages persist at low diversity for some period of time after their initial origins ('phylogenetic fuses'; see ref. 10) before undergoing evolutionary explosions 1,11. Principal among these scenarios is the 'long-fuse model' 1 , which postulates an extended lag between the Cretaceous origins of the orders and the first split among their living representatives (crown groups) immediately after the K/T boundary 8. Some older molecular studies advocate a 'short-fuse model' of diversification 1 , where even the basal crown-group divergences within some of the larger placental orders occur well within the Cretaceous period 5-7. A partial molecular phylogeny emphasizing divergences among placental orders suggested that over 20 lineages with extant descendants (henceforth, 'extant lineages') survived the K/T boundary 8. However, the total number of extant lineages that pre-date the extinction event and whether or not they radiated immediately after it remain unknown. The fossil record alone does not provide direct answers to these questions. It does reveal a strong pulse of diversification in stem eutherians immediately after the K/T boundary 4,12 , but few of the known Palaeocene taxa can be placed securely within the crown groups of extant orders comprising Placentalia 4. The latter only rise to prominence in fossils known from the Early Eocene epoch onwards (,50 Myr ago) after a major faunal reorganization 4,13,14. The geographical patchiness of the record complicates interpretations of this near-absence of Palaeocene crown-group fossils 14-16 : were these clades radiating throughout the Palaeocene epoch in parts of the world where the fossil record is less well known; had they not yet originated; or did they have very long fuses, remaining at low diversity until the major turnover at the start of the Eocene epoch? The pattern of diversification rates through time, to which little attention has been paid so far, might hold the key to answering these questions. If the Cretaceous fauna inhibited mammalian diversification , as is commonly assumed 1 , and all mammalian lineages were able to radiate after their extinction, then there should be a significant increase in the net per-lineage rate of extant mammalian diversification , r (the difference between the per-lineage speciation and extinction rates), immediately after the K/T mass extinction. This hypothesis, along with the explosive, long-and short-fuse models, can be tested using densely sampled phylogenies of extant species, which contain information about the history of their diversification rates 17-20. Using modern supertree algorithms 21,22 , we construct the first virtually complete species-level phylogeny of extant mammals from over 2,500 partial estimates, and estimate divergence times (with confidence intervals) throughout it using a 66-gene alignment in conjunction with 30 cladistically robust fossil calibration points. Our analyses of the supertree indicate that the principal splits underlying the diversification of the extant lineages occurred (1) from 100-85 Myr ago with the origins of the extant orders, and (2) in or after the Early Eocene (agreeing with the upturn in their diversity known from the fossil record 4,13,14), but not immediately after the K/T boundary, where diversification rates are unchanged. Our findings-that more extant placental lineages survived the K/T boundary than previously recognized and that fewer arose immediately after it than previously suspected-extend the phylogenetic fuses of many extant orders and indicate that the end-Cretaceous mass extinction event had, at best, a minor role in driving the diversification of the present-day mam-malian lineages. A supertree with divergence times for extant mammals The supertree contains 4,510 of the 4,554 extant species recorded in ref. 23, making it 99.0% complete at the species level (Fig. 1; see also
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The dwarf and mouse lemurs of Madagascar are two very species-rich lemur genera, yet there is a relative paucity of information on this primate family in published literature. In this first ever treatment of the Cheirogaleidae, international experts are brought together to review and integrate our current knowledge of the behaviour, physiology, ecology, genetics and biogeography of these species. A wide range of direct and indirect research methods that are currently used to study these cryptic nocturnal solitary foragers are described. By uniting often disparate research on captive and free-ranging taxa and synthesising recent methodological advances, this book provides new insights that will encourage further studies of this fascinating primate family. This synthesis will provide an incentive for more integrative studies of the Cheirogaleidae in captivity and in the wild, enabling the impacts of deforestation and other factors to be identified and directions for future conservation efforts to be established.
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Studies of soft tissue effects on joint mobility in extant animals can help to constrain hypotheses about joint mobility in extinct animals. However, joint mobility must be considered in three dimensions simultaneously, and applications of mobility data to extinct taxa require both a phylogenetically informed reconstruction of articular morphology and justifications for why specific structures’ effects on mobility are inferred to be similar. We manipulated cadaveric hip joints of common quail and recorded biplanar fluoroscopic videos to measure a ‘ligamentous’ range of motion (ROM), which was then compared to an ‘osteological’ ROM on a ROM map. Nearly 95% of the joint poses predicted to be possible at the hip based on osteological manipulation were rendered impossible by ligamentous constraints. Because the hip joint capsule reliably includes a ventral ligamentous thickening in extant diapsids, the hip abduction of extinct ornithodirans with an offset femoral head and thin articular cartilage was probably similarly constrained by ligaments as that of birds. Consequently, in the absence of extraordinary evidence to the contrary, our analysis casts doubt on the ‘batlike’ hip pose traditionally inferred for pterosaurs and basal maniraptorans, and underscores that reconstructions of joint mobility based on manipulations of bones alone can be misleading. © 2018 The Author(s) Published by the Royal Society. All rights reserved.
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Background Sciuromorpha (squirrels and close relatives) are diverse in terms of body size and locomotor behavior. Individual species are specialized to perform climbing, gliding or digging behavior, the latter being the result of multiple independent evolutionary acquisitions. Each lifestyle involves characteristic loading patterns acting on the bones of sciuromorphs. Trabecular bone, as part of the bone inner structure, adapts to such loading patterns. This network of thin bony struts is subject to bone modeling, and therefore reflects habitual loading throughout lifetime. The present study investigates the effect of body size and lifestyle on trabecular structure in Sciuromorpha. Methods Based upon high-resolution computed tomography scans, the femoral head 3D inner microstructure of 69 sciuromorph species was analyzed. Species were assigned to one of the following lifestyle categories: arboreal, aerial, fossorial and semifossorial. A cubic volume of interest was selected in the center of each femoral head and analyzed by extraction of various parameters that characterize trabecular architecture (degree of anisotropy, bone volume fraction, connectivity density, trabecular thickness, trabecular separation, bone surface density and main trabecular orientation). Our analysis included evaluation of the allometric signals and lifestyle-related adaptation in the trabecular parameters. Results We show that bone surface density, bone volume fraction, and connectivity density are subject to positive allometry, and degree of anisotropy, trabecular thickness, and trabecular separation to negative allometry. The parameters connectivity density, bone surface density, trabecular thickness, and trabecular separation show functional signals which are related to locomotor behavior. Aerial species are distinguished from fossorial ones by a higher trabecular thickness, lower connectivity density and lower bone surface density. Arboreal species are distinguished from semifossorial ones by a higher trabecular separation. Conclusion This study on sciuromorph trabeculae supplements the few non-primate studies on lifestyle-related functional adaptation of trabecular bone. We show that the architecture of the femoral head trabeculae in Sciuromorpha correlates with body mass and locomotor habits. Our findings provide a new basis for experimental research focused on functional significance of bone inner microstructure. Electronic supplementary material The online version of this article (10.1186/s40851-018-0093-z) contains supplementary material, which is available to authorized users.
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The gaits of the adult grey mouse lemur Microcebus murinus were studied during treadmill locomotion over a large range of velocities. The locomotion sequences were analysed to determine the gait and the various spatiotemporal gait parameters of the limbs. We found that velocity adjustments are accounted for differently by stride frequency and stride length depending on whether the animal showed a symmetrical or an asymmetrical gait. When using symmetrical gaits the increase in velocity is associated with a constant contribution of the stride length and stride frequency; the increase of the stride frequency being always lower. When using asymmetrical gaits, the increase in velocity is mainly assured by an increase in the stride length which tends to decrease with increasing velocity. A reduction in both stance time and swing time contributed to the increase in stride frequency for both gaits, though with a major contribution from the decrease in stance time. The pattern of locomotion obtained in a normal young adult mouse lemurs can be used as a template for studying locomotor control deficits during aging or in different environments such as arboreal ones which likely modify the kinematics of locomotion.
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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.
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The phylogeny of eutherian mammals contains some of the most recalcitrant nodes in the tetrapod tree of life. We combined comprehensive taxon and character sampling to explore three of the most debated interordinal relationships among placental mammals. We performed in silico extraction of ultraconserved element loci from 72 published genomes and invitro enrichment and sequencing of ultraconserved elements from 28 additional mammals, resulting in alignments of 3,787 loci. We analyzed these data using concatenated and multispecies coalescent phylogenetic approaches, topological tests, and exploration of support among individual loci to identify the root of Eutheria and the sister groups of tree shrews (Scandentia) and horses (Perissodactyla). Individual loci provided weak, but often consistent support for topological hypotheses. Although many gene trees lacked accepted species-tree relationships, summary coalescent topologies were largely consistent with inferences from concatenation. At the root of Eutheria, we identified consistent support for a sister relationship between Xenarthra and Afrotheria (i.e., Atlantogenata). At the other nodes of interest, support was less consistent. We suggest Scandentia is the sister of Primatomorpha (Euarchonta), but we failed to reject a sister relationship between Scandentia and Glires. Similarly, we suggest Perissodactyla is sister to Cetartiodactyla (Euungulata), but a sister relationship between Perissodactyla and Chiroptera remains plausible.
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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.
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Numerous factors have stimulated new enthusiasm for understanding the process of primate origins, including new fossil discoveries, improvements to methods for analyzing molecular data, and technological advances. These novel approaches have led to a better appreciation of the complexities of early primate evolution. Eight fundamental questions provide a framework for thinking about these issues. Among these topics are the phylogenetic position of Primates in Mammalia and the membership of particular fossil groups in the order. Also of central interest are questions about early primate ecology and anatomy such as the ancestral body mass, diet, locomotor mode, interactions with predators, and brain size and form. And finally, considerations of the paleontological record need to be informed by the most relevant living models, which help flesh out the story that is being told by fossils. Although much is known about all of these areas, fundamental questions still remain.
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Palaechthonid plesiadapiforms from the Palaeocene of western North America have long been recognized as among the oldest and most primitive euarchontan mammals, a group that includes extant primates, colugos and treeshrews. Despite their relatively sparse fossil record, palaechthonids have played an important role in discussions surrounding adaptive scenarios for primate origins for nearly a half-century. Likewise, palaechthonids have been considered important for understanding relationships among plesiadapiforms, with members of the group proposed as plausible ancestors of Paromomyidae and Microsyopidae. Here, we describe a dentally associated partial skeleton of Torrejonia wilsoni from the early Palaeocene (approx. 62 Ma) of New Mexico, which is the oldest known plesiadapiform skeleton and the first postcranial elements recovered for a palaechthonid. Results from a cladistic analysis that includes new data from this skeleton suggest that palaechthonids are a paraphyletic group of stem primates, and that T. wilsoni is most closely related to paromomyids. New evidence from the appendicular skeleton of T. wilsoni fails to support an influential hypothesis based on inferences from craniodental morphology that palaechthonids were terrestrial. Instead, the postcranium of T. wilsoni indicates that it was similar to that of all other plesiadapiforms for which skeletons have been recovered in having distinct specializations consistent with arboreality.
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Differences in body size and in the use of arboreal strata limit the climbing behaviour and performance of didelphids. Similarly to primates, the arboreal canopy dweller, Caluromys philander exhibits a diagonal-sequence gait. In contrast, terrestrial didelphids use a symmetrical lateral sequence in horizontal locomotion. Postural behaviour along thin supports may allow understanding the mechanisms behind the higher performance of arboreal didelphids climbing. Here in, we describe and compare gait sequence and postural behaviour of seven didelphids climbing a slender and flexible vertical support. Animals were stimulated to climb a vertical support of 1.25 cm diameter. Postural behaviour was qualitatively described for each species in the cycle of maximum velocity by a frame-by-frame analysis of gait cycles, evaluating (1) movements of the tail, (2) posture of hand and wrist when grasping, (3) distance of the body to the support, (4) lateral swinging of the body, (5) orientation of the head, (6) limb posture, and (7) stride cycle. Only arboreal species were capable of climbing with only two limbs grasping the support, keeping a straight body orientation at some distance from the support, and sustaining a more constant and regular climbing velocity. The tail played a role in didelphids with better climbing performance (i.e., higher relative velocity), counteracting the lateral swinging of the body, helping with the animal balance. However, the prehensile ability of the tail was not used in climbing. The most stunning result is that all didelphids grasped the rope between digits 2-3, a schizaxonic grasp, involving a neutral hand orientation regarding the ulna. The didelphids protracted the humerus at forelimb touchdown, and the angle between the arm and the horizontal body axis was greater than 90°. The same postures were already observed in horizontal locomotion of C. philander, Monodelphis domestica, and primates. Locomotory and postural adaptations for an arboreal lifestyle in didelphids seem to be limited to small to medium body sizes, up to the size of species of Caluromys. The arboreal locomotion of didelphids is an important key to understand adaptation and evolution of mammals to an arboreal niche, and the comparison with small primates may help to identify adaptive convergence to arboreal locomotion. © 2016, Universidade Federal do Rio de Janeiro (UFRJ). All rights reserved.
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The acacia rat Thallomys paedulcus is a small arboreal rodent, extensively dependent on Acacia sp. trees. In order to understand the arboreal locomotor adaptations of the species we examined their gaits in arboreal locomotion (i.e. diagonality, duty factor, duty factor index, velocity, and stride length and frequency). For these purposes, we filmed 12 captive specimens on simulated arboreal substrates of variable sizes (2mm, 5mm, 10mm, 25mm) and inclinations (00 and 450). Acacia rats employed slow, symmetrical gaits with lower diagonality on the smaller substrates, which were progressively substituted by faster, asymmetrical half-bounding gaits on larger substrates. In general, inclination had no impact on gait metrics, except that ascents were slower than horizontal locomotion. Velocity increase was regulated primarily by an increase in stride frequency, a pattern encountered in many small mammals, although stride length contributed significantly, as well. These locomotor adaptations serve as a behavioural mechanism to cope with the challenges of the arboreal milieu. They appear to provide stability and enable safe negotiation of arboreal substrates, ultimately leading to the successful exploitation of Acacia trees in their natural habitat.
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Very shortly after the disappearance of the non-avian dinosaurs, the first mammals that had features similar to those of primates started appearing. These first primitive forms went on to spawn a rich diversity of plesiadapiforms, often referred to as archaic primates. Like many living primates, plesiadapiforms were small arboreal animals that generally ate fruit, insects, and, occasionally, leaves. However, this group lacked several diagnostic features of euprimates. They also had extraordinarily diverse specializations, represented in eleven families and more than 140 species, which, in some cases, were like nothing seen since in the primate order. Plesiadapiforms are known from all three Northern continents, with representatives that persisted until at least 37 million years ago. In this article we provide a summary of the incredible diversity of plesiadapiform morphology and adaptations, reviewing our knowledge of all eleven families. We also discuss the challenges that remain in our understanding of their ecology and evolution.
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Body size imposes significant constraints on arboreal locomotion. Despite the wealth of research in larger arboreal mammals, there is a lack of data on arboreal gaits of small mammals. In this context, the present study explores arboreal locomotion in one of the smallest rodents, the Eurasian harvest mice Micromys minutus (~10g). We examined gait metrics (i.e. diagonality, duty factor, duty factor index, velocity, stride length and stride frequency) of 6 adult male mice on simulated arboreal substrates of different sizes (2 mm, 5 mm, 10 mm, 25 mm) and inclinations (00 and 450). Micromys minutus employed slow, lateral-sequence symmetrical gaits on the smaller substrates, which shifted to progressively faster symmetrical gaits of higher diagonality on larger substrates. Both ascents and descents were associated with a higher diagonality, and ascents with a higher duty factor index compared to horizontal locomotion, underscoring the role of the grasping hind feet. Velocity increase was brought about primarily by an increase in stride frequency, a pattern often encountered in other small mammals, with a secondary and significant contribution of stride length. These findings indicate that, except for velocity and the way it is regulated, there are no significant differences in gait metrics between larger and smaller arboreal mammals. Moreover, the locomotor adaptations of Eurasian harvest mice represent behavioral mechanisms that promote stable, safe and continuous navigation along slender substrates, and ultimately contribute to the successful exploitation of the arboreal milieu.
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Vertical stratification of the arboreal habitat allows the coexistence of several species in a given area, because the complex arboreal strata can be used in different ways by arboreal and scansorial mammals. The present report experimentally investigated the gait metrics on different arboreal substrates, of three sympatric rodents living in a deciduous forest in Poznań, Poland. Arboreal locomotion was compared between the burrowing striped field mouse, Apodemus agrarius, the scansorial bank vole, Myodes glareolus, and the more arboreal yellow-necked mouse, Apodemus flavicollis. We filmed two wild-caught individuals from each species walking on four different substrate diameters (2mm, 5mm, 10mm, 25mm) and three different inclinations (45° descending, horizontal, 45° ascending) at 240 fps and collected a set of gait parameters from a total of 273 complete cycles. Our results did not demonstrate clear relationships between arboreal locomotion and the ecology of the three species. Only A. flavicollis exhibited locomotor features partly associated with arboreal competence, including lower velocity and diagonality on narrow substrates and asymmetrical gaits on wider ones. On the other hand, the two Apodemus species, despite their different ecologies, shared a few locomotor similarities, such as velocity regulation primarily by stride frequency, and similar effects of substrate size and inclination on diagonality, duty factor, and duty factor index indicating the possibility of a phylogenetic signal. Because the selected gait parameters provided limited insight into the ability of small mammals to move competently through an arboreal habitat, these findings indicate that the relationship between behaviour and ecology is complex.
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Pedal grasping evolution in euarchontan mammals is of great importance as it bears on the adaptive significance of specialized hallucal grasping and arboreal niche use related to the group differentiation. Basally divergent arboreal tupaiid treeshrews are very suitable for testing pedal grasping modes and associated substrate correlates and provide insights on euarchontan pedal evolution. For these purposes we filmed wild-caught Dendrogale murina from Vietnam and analyzed their foot mechanisms. Our observations showed that hallucal grasp was moderately used and was mainly associated with small and horizontal substrates. Convergent grasp was frequently used on medium-sized and horizontal substrates whereas claws were related to large and vertical substrates. In addition, the foot was frequently inverted and mainly placed in a semiplantigrade position. Inversion and semiplantigrady dominated on small, medium-sized and horizontal substrates but decreased on larger substrates with increased inclinations. The observed pedal mechanism probably represents a derived condition, where hallucal grasping tends to become slightly restrained, compared to the primitive euarchontan (and scandentian) pedal grasping mechanism. Furthermore, it hallmarks an early stage in tupaiid evolution towards a more constrained pedal grasping. This further substantiates pedal grasping plasticity within euarchontan mammals and highlights the strong relation between a hallucal grasping mechanism and the frequent and primary use of small slender substrates.
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Over the last decade, we have learned much about the anatomy, evolutionary history, and biomechanics of the extant sloths. However, most of this work has involved studying sloths in controlled conditions, and few studies have explored how these animals are behaving in a naturalistic setting. In this study, we integrate positional activities in naturalistic conditions with kinematic and kinetic observations collected on a simulated runway in order to best capture the biomechanical behavior of Linnaeus’s Two-toed Sloths. We confirm that the dominant positional behaviors consist of hanging below the support using a combination of forelimbs and hindlimbs, and walking quadrupedally below the branches. The majority of these behaviors occur on horizontal substrates that are approximately 5-10 cm in diameter. The kinematics of suspensory walking observed both in the naturalistic settings and on simulated arboreal runways are dominated by movement of the proximal limb elements, while distal limb elements tend to show little excursion. Joint kinematics are similar between the naturalistic setting and the simulated runway, but movements of the shoulder and hip tend to be exaggerated while moving in simulated conditions. Kinetic patterns of the two-toed sloth can be explained almost entirely by considering them as an inverted linked strut. However, medially-directed forces towards the substrate were more frequent than expected in the forelimb, which may help sloths maintain a better “grip” on the substrate. This research serves as a model of how to gain a comprehensive understanding of the functional-adaptive profile of a particular species.
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Debates on early euprimate evolution are related to the understanding of the ecological context that promoted their unique adaptations. Currently, these discussions mainly revolve around the habitual use of the small-branch niche or the frequent utilization of wider, and probably, strongly inclined substrates by euprimate ancestors. The current fossil evidence implies a diversity of arboreal quadrupedal behaviors for these early euprimates, associated with the use of various types of substrates. However, inferring the positional behavior of early euprimates based exclusively on fossils fails to unravel the positional flexibility in terms of modes and substrate use, which is important for understanding key adaptations related to limb postures. Following previous research, we studied the positional behavior, substrate use and pedal grasping modes of the marsupial feathertail gliders to investigate patterns of arboreal behavior that may be analogous to those exhibited by early euprimate ancestors. For the purposes of the current study, we observed and filmed 15 male and 20 female captive adult feathertail gliders Acrobates pygmaeus (Marsupialia: Diprotodontia: Acrobatidae) in a large enclosure in the Nocturnal Pavilion of Nowe Zoo, Poznań, Poland. Our observations demonstrated a strong preference for small and for horizontal substrates, avoidance of large and of vertical ones, a diverse positional repertoire mainly composed of quadrupedalism, clambering, climbing and gliding, the last occurring from small and oblique and vertical substrates, and the dominant use of hallucal grasping, especially on small, horizontal and oblique substrates. We thus consider that the generalized profile of A. pygmaeus could fit in a stage where the euarchontan heritage of vertical clawed activities on large substrates has decreased in favor of the use of small moderately inclined substrates efficiently negotiated by diagonal sequence quadrupedalism and handled via an apparently powerful hallucal grasp. Competent use of small substrates could have further expanded into small vertical substrates, which would progressively serve as new climbing platforms and takeoff perches for unspecialized leaping. We feel that this stage may have occurred early in euprimate evolution, as small body size likely provided the necessary behavioral flexibility to exploit various niches. Depending on alternative scenarios, it could represent that of the common ancestor of euprimates or be rooted at the base of strepsirrhine evolution. This study underscores the important of analyzing the behavior of extant models to infer the locomotor evolution of euarchontans, primates or euprimates.
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Colugos (order Dermoptera) are medium-sized nocturnal arboreal eutherian euarchontan mammals, which glide, climb vertically and hang from different arboreal substrates in the rainforests of Southeast Asia. Their close phylogenetic position to either Primates (as Primatomorpha) or Scandentia (as Sundatheria) renders them significant for understanding evolutionary-adaptive trends of key features within the Euarchonta (primates, scandentia, dermoptera, and plesiadapiformes). In this context, we studied foot positional, postural, and grasping patterns in relation to substrate use in free-ranging Sunda colugos (Galeopterus variegatus) in west Java, Indonesia. On large, strongly inclined substrates, colugos primarily used claw climbing and clinging activities, with a dorsiflexed, abducted, and everted foot using an abducted clawed grasp and abducted hallux. On small, less inclined substrates, colugos habitually used suspensory locomotion and postures with pedal plantarflexion, adduction, inversion, and an adducted clawed grasp and adducted hallux. The morphofunctional similarity of the colugo foot with that of early euarchontans suggests comparable behaviors at the base of euarchontan evolution. Furthermore, the functional-adaptive significance of these behaviors is further investigated under different phylogenetic scenarios, linking dermopterans to either scandentians or primates. Our findings underscore the importance of similar behavioral studies for examining functional-adaptive evolutionary scenarios.
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The importance of locomotion to evolutionary fitness has led to extensive study of primate locomotor behavior, morphology and ecology. Most previous research has focused on adult primates, but in the last few decades, increased attention to locomotor development has provided new insights toward our broader understanding of primate adaptation and evolution. Here, we review the contributions of this body of work from three basic perspectives. First, we assess possible determinants on the timing of locomotor independence, an important life history event. Significant influences on timing of locomotor independence include adult female body mass, age at weaning, and especially relative brain size, a significant predictor of other primate life history variables. Additionally, we found significant phylogenetic differences in the timing of locomotor independence, even accounting for these influences. Second, we discuss how structural aspects of primate growth may enhance the locomotor performance and safety of young primates, despite their inherent neuromotor and musculoskeletal limitations. For example, compared to adults, growing primates have greater muscle mechanical advantage, greater bone robusticity, and larger extremities with relatively long digits. Third, focusing on primate quadrupedalism, we provide examples that illustrate how ontogenetic transitions in morphology and locomotion can serve as a model system for testing broader principles underlying primate locomotor biomechanics. This approach has led to a better understanding of the key features that contribute to primates’ stride characteristics, gait patterns, limb force distribution, and limb postures. We have learned a great deal from the study of locomotor ontogeny, but there is much left to explore. We conclude by offering guidelines for future research, both in the laboratory and the field.
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The fascicular architecture of skeletal muscle dictates functional parameters such as force production and contractile velocity. Muscle microarchitecture is typically determined by means of manual dissection, a technique that is inherently destructive to specimens. Furthermore, fascicle lengths and pennation angles are commonly assessed at only a limited number of sampling sites per muscle. We present the results of a digital technique to non-destructively assess muscle architectural variables for three jaw-adductor muscles within a specimen of the cercopithecine primate Macaca fascicularis (crab-eating macaque). The specimen is first subjected to a contrast-enhanced staining protocol to increase the density of internal soft tissues. High-resolution µCT scans are then collected and segmented to isolate individual muscles. A textural orientation algorithm is then applied to each muscle volume to reconstruct constituent muscle fascicles in three dimensions. Using this technique, we report muscle volume, fascicle length, angle of pennation, and physiological cross-sectional area (PCSA) for each muscle. These data are compared to results collected using traditional dissection of the contralateral muscles. Reconstructions of muscle volume and pennation angle closely correspond to the dissection results. The degree of similarity between measurements of fascicle length and PCSA varies between muscles, with temporalis demonstrating the greatest disparity between techniques; likely reflecting the complex geometry and fascicular arrangement of this muscle. The described technique samples a much larger number of fascicles than had previously been possible and non-destructively investigates the internal architecture of preserved specimens. We conclude that this approach demonstrates great potential for quantifying muscle internal architecture. Anat Rec, 301:363–377, 2018. © 2018 Wiley Periodicals, Inc.
Book
Phylogenetic comparative approaches are powerful analytical tools for making evolutionary inferences from interspecific data and phylogenies. The phylogenetic toolkit available to evolutionary biologists is currently growing at an incredible speed, but most methodological papers are published in the specialized statistical literature and many are incomprehensible for the user community. This textbook provides an overview of several newly developed phylogenetic comparative methods that allow to investigate a broad array of questions on how phenotypic characters evolve along the branches of phylogeny and how such mechanisms shape complex animal communities and interspecific interactions. The individual chapters were written by the leading experts in the field and using a language that is accessible for practicing evolutionary biologists. The authors carefully explain the philosophy behind different methodologies and provide pointers – mostly using a dynamically developing online interface – on how these methods can be implemented in practice. These “conceptual” and “practical” materials are essential for expanding the qualification of both students and scientists, but also offer a valuable resource for educators.
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The fossil record of early primates is largely comprised of dentitions. While teeth can indicate phylogenetic relationships and dietary preferences, they say little about hypotheses pertaining to the positional behavior or substrate preference of the ancestral crown primate. Here we report the discovery of a talus bone of the dentally primitive fossil euprimate Donrussellia provincialis. Our comparisons and analyses indicate that this talus is more primitive than that of other euprimates. It lacks features exclusive to strepsirrhines, like a large medial tibial facet and a sloping fibular facet. It also lacks the medially positioned flexor-fibularis groove of extant haplorhines. In these respects, the talus of D. provincialis comes surprisingly close to that of the pen-tailed treeshrew, Ptilocercus lowii, and extinct plesiadapiforms for which tali are known. However, it differs from P. lowii and is more like other early euprimates in exhibiting an expanded posterior trochlear shelf and deep talar body. In overall form, the bone approximates more leaping reliant euprimates. The phylogenetically basal signal from the new fossil is confirmed with cladistic analyses of two different character matrices, which place D. provincialis as the most basal strepsirrhine when the new tarsal data are included. Interpreting our results in the context of other recent discoveries, we conclude that the lineage leading to the ancestral euprimate had already become somewhat leaping specialized, while certain specializations for the small branch niche came after crown primates began to radiate.
Chapter
To understand the hand of living primates from an adaptive perspective, data on the morphological pattern of the earliest primates is required. This chapter discusses what is known about the early evolution of primate hands based on fossils of Paleogene plesiadapiforms (potential stemprimates), adapiforms, omomyiforms, and anthropoids. Implications of these data for understanding locomotor transitions during the origin and early evolutionary history of primates is considered. Though the number of plesiadapiform species known from well preserved postcranial skeletons remains small, known species are similar to extant primates in both their intrinsic hand proportions and hand-to-body size proportions. Nonetheless, the presence of claws and a different metacarpophalangeal form in plesiadapiforms suggests grasping mechanics unlike those of either extant primates or Eocene adapiforms and omomyiforms. We find that non-adapine adapiforms and the basal omomyiform Teilhardina resemble tarsiers and some galagos in having extremely elongated proximal phalanges and digit rays relative to metacarpals. Looking at hand-to-body size proportions, all sampled adapiforms appear to be average compared to extant primate diversity, whereas Teilhardina seems to have had extremely large hands for its size like tarsiers and Daubentonia. Non-adapine adapiforms and omomyiforms exhibit carpal features suggesting more limited dorsiflexion, greater ulnar deviation, and a more habitually divergent (or abducted) pollex than observed plesiadapiforms. Together, features differentiating adapiforms and omomyiforms from plesiadapiforms indicate increased reliance on vertical clinging and grasp-leaping, possibly in combination with predatory behaviors in ancestral euprimates.
Article
As the smallest living primate, the mouse lemur is a suitable model for reconstructing the locomotor mechanisms by which primate ancestors might have responded to the challenges of an arboreal environment. In this study, we tested the effects of substrate diameter and orientation on quadrupedal gait kinematics in mouse lemurs (Microcebus murinus). Mouse lemurs highly preferred asymmetrical to symmetrical gaits as they moved across a flat board and poles of three diameters (2.5, 1.0, and 0.5 cm), set at horizontal, 30° inclined, and 30° declined orientations. During symmetrical gaits, mouse lemurs used diagonal sequence walking and ambling gaits on the same substrates and at the same duty factors for which some similarly sized nonprimate mammals use lateral sequence gaits, suggesting that reliance on diagonal sequence walking in primates may not be explicitly a response to body size relative to substrate diameter. When using asymmetrical gaits, kinematic adjustments to small diameter and/or nonhorizontal substrates included a preference for transverse gallops over other gaits, the avoidance of whole-body suspensions, increases in limb contact duration, and increases in the time interval between the landing of trailing and leading limbs. All of these adjustments are consistent with increasing locomotor stability by dampening center of mass movements and reducing the forces imparted to the substrate. Like mouse lemurs, small-bodied ancestral primates likely used symmetrical gaits occasionally, but more frequently used asymmetrical gaits that were adjusted in response to challenging substrates. Therefore, asymmetrical gait dynamics should be incorporated into hypotheses addressing early primate locomotor evolution.
Article
The Common tree shrew was studied over three and half years in tropical rainforest habitats in West Malaysia, using various trapping methods. It was more terrestrial than arboreal and the overall sex ratio remained close to unity. The main reproductive period was between February and June and the litter size invariably two. Some females bred more than once a season and the age at first pregnancy was seven months. Growth rate was measured from weaning to adult weight. Density varied from about two to five animals per hectare. The monthly survival rate was 0·75–0·93, and the maximum age recorded was over 4 years. The main period of emigration or mortality was during the breeding period or the North East Monsoon. The main food was invertebrates with some vegetable matter. These results support captive studies that T. glis are territorial with about two pairs per hectare prior to breeding. Predation did not seem to be important. Although survival resembled that of temperate insectivores, the litter size was more like lower primates. The annual breeding coincided with the abundance of invertebrates after the dry season, also shown by insectivorous birds. The low production of young was compensated for by the relatively high longevity of adults.
Chapter
The Order Primates is characterized by a unique suite of cranial and postcranial features that may have evolved for visual predation on insects or exploitation of fruits in a small-branch milieu [see Cartmill (1992) for recent review]. Compared to more generalized mammals like tree shrews, primates possess a relatively larger brain with a more developed visual area and more reduced olfactory bulbs, orbits that are more approximated and more convergent with one another, and grasping hands and feet that bear nails instead of claws (Cartmill, 1970, 1972, 1974a,b, 1992; Le Gros Clark, 1959, 1963; Martin, 1986; Wood Jones, 1916).