Evolution of arboreality and fossoriality in squirrels and aplodontid rodents: Insights from the semicircular canals of fossil rodents

Reconstructing locomotor behaviour for fossil animals is typically done with postcranial elements. However, for species only known from cranial material, locomotor behaviour is difficult to reconstruct. The semicircular canals (SCCs) in the inner ear provide insight into an animal's locomotor agility. A relationship exists between the size of the SCCs relative to body mass and the jerkiness of an animal's locomotion. Additionally, studies have also demonstrated a relationship between SCC orthogonality and angular head velocity. Here, we employ two metrics for reconstructing locomotor agility, radius of curvature dimensions and SCC orthogonality, in a sample of twelve fossil rodents from the families Ischyromyidae, Sciuridae and Aplodontidae. The method utilizing radius of curvature dimensions provided a reconstruction of fossil rodent locomotor behaviour that is more consistent with previous studies assessing fossil rodent locomotor behaviour compared to the method based on SCC orthogonality. Previous work on ischyromyids suggests that this group displayed a variety of locomotor modes. Members of Paramyinae and Ischyromyinae have relatively smaller SCCs and are reconstructed to be relatively slower compared to members of Reithroparamyinae. Early members of the Sciuroidea clade including the sciurid Cedromus wilsoni and the aplodontid Prosciurus relictus are reconstructed to be more agile than ischyromyids, in the range of extant arboreal squirrels. This reconstruction supports previous inferences that arboreality was likely an ancestral trait for this group. Derived members of Sciuridae and Aplodontidae vary in agility scores. The fossil squirrel Protosciurus cf. rachelae is inferred from postcranial material as arboreal, which is in agreement with its high agility, in the range of extant arboreal squirrels. In contrast, the fossil aplodontid Mesogaulus paniensis has a relatively low agility score, similar to the fossorial Aplodontia rufa, the only living aplodontid rodent. This result is in agreement with its postcranial reconstruction as fossorial and with previous indications that early aplodontids were more arboreal than their burrowing descendants.     

Comparative study of notoungulate (Placentalia,Mammalia) bony labyrinths and new phylogenetically informative inner ear characters

The phylogenetic relationships of notoungulates, an extinct group of predominantly South American herbivores, remain poorly resolved with respect to both other placental mammals and among one another. Most previous phylogenetic analyses of notoungulates have not included characters of the internal cranium, not least because few such features, including the bony labyrinth, have been described for members of the group. Here we describe the inner ears of the notoungulates Altitypotherium chucalensis (Mesotheriidae), Pachyrukhos moyani (Hegetotheriidae) and Cochilius sp. (Interatheriidae) based on reconstructions of bony labyrinths obtained from computed tomography imagery. Comparisons of the bony labyrinths of these taxa with the basally diverging notoungulate Notostylops murinus (Notostylopidae), an isolated petrosal from Itaboraí, Brazil, referred to Notoungulata, and six therian outgroups, yielded an inner ear character matrix of 25 potentially phylogenetically informative characters, 14 of them novel to this study. Two equivocally optimized character states potentially support a pairing of Mesotheriidae and Hegetotheriidae, whereas four others may be diagnostic of Notoungulata. Three additional characters are potentially informative for diagnosing more inclusive clades: one for crown Placentalia; another for a clade containing Kulbeckia, Zalambdalestes, and Placentalia; and a third for Eutheria (crown Placentalia plus stem taxa). Several other characters are apomorphic for at least one notoungulate in our study and are of potential interest for broader taxonomic sampling within Notoungulata to clarify currently enigmatic interrelationships. Measures of the semicircular canals were used to infer agility (e.g. capable of quick movements vs. lethargic movements) of these taxa. Agility scores calculated from these data generally corroborate interpretations based on postcranial remains of these or closely related species. We provide estimates of the low‐frequency hearing limits in notoungulates based on the ratio of radii of the apical and basal turns of the cochlea. These limits range from 15 Hz in Notostylops to 149 Hz in Pachyrukhos, values comparable to the Asian elephant (Elephas maximus) and the California sea lion (Zalophus californianus) when hearing in air, respectively.     

Eocene Paleoecology of Adapis parisiensis (Primate,Adapidae): From Inner Ear to Lifestyle

European adapids, especially Adapis parisiensis, have been extensively studied over the past two centuries, essentially for taxonomic and phylogenetic purposes. Analyses of dental, cranial, and postcranial morphology have led to various hypotheses about the diet, locomotion, and lifestyle of this fossil primate species. As the morphology of Adapis parisiensis is not directly comparable to any extant species, some interpretations are still debated. The inner ear is crucial to several functional parameters, such as auditory acuity, balance, agility, orientation, and head motion speed during locomotion. We examined the inner ear morphology of Adapis parisiensis in order to make some functional inferences, using μCT techniques to access the internal morphology without damaging the fossil specimens. We analyzed the length and shape of the cochlea, the size of the oval window, and the size and orientation of the semicircular canals of seven Adapis parisiensis crania. Results indicate that the species was more sensitive to high frequencies than low frequencies. Results for locomotion style are different, depending on the method used. Results about the coefficient of agility are in good agreement with previous studies, proposing a slow/medium slow locomotion for the fossil species. In contrast, angular velocity magnitude (AVM) results show a great range of variation in the locomotor repertory for Adapis parisiensis, probably indicating that the model used is not adapted to the study of the fossil record. A comparison to measurements of extant strepsirhines leads us to conclude that Adapis parisiensis was probably monogamous and solitary, with a small home range. Anat Rec, 300:1576–1588, 2017. © 2017 Wiley Periodicals, Inc.     

Anatomical study of the auditory region of Arctotherium tarijense (Ursidae,Tremarctinae), an extinct short‐faced bear from the Pleistocene of South America

Here we present the most detailed morphological study of the auditory region of a tremarctinae bear, Arctotherium tarijense Ameghino. In addition, we provide new anatomical information of the Tremarctinae inner ear, such as coplanarity and deviation from orthogonality of the semicircular canals, as an approach to infer the head movements which encountered the extinct forms in locomotion. Based on morphological comparisons, A. tarijense exhibits the following particular features: the cavum tympani presents the highest relative volume compared with other ursids; the processus paraoccipitalis has a foramen that is absent in other tremarctines; there is only one (ventral) recess in the anterior region of the cavum tympani; and the recessus epytimpanicus is the smallest for all ursids studied. In relation to the inner ear, A. tarijense shows the lowest values of orthogonality deviation and highest scores of locomotor agility. Based on this, is possible to make a preliminary proposal that this species had a relative high vestibular sensibility and therefore a better ability to explore different kind of habitats. However, this hypothesis might be contrasted among bears taking into account the orientation of each semicircular canal in a phylogenetic framework.     

Limb bone morphology,bone strength,and cursoriality in lagomorphs

The primary aim of this study is to broadly evaluate the relationship between cursoriality (i.e. anatomical and physiological specialization for running) and limb bone morphology in lagomorphs. Relative to most previous studies of cursoriality, our focus on a size‐restricted, taxonomically narrow group of mammals permits us to evaluate the degree to which ‘cursorial specialization’ affects locomotor anatomy independently of broader allometric and phylogenetic trends that might obscure such a relationship. We collected linear morphometrics and μCT data on 737 limb bones covering three lagomorph species that differ in degree of cursoriality: pikas (Ochotona princeps, non‐cursorial), jackrabbits (Lepus californicus, highly cursorial), and rabbits (Sylvilagus bachmani, level of cursoriality intermediate between pikas and jackrabbits). We evaluated two hypotheses: cursoriality should be associated with (i) lower limb joint mechanical advantage (i.e. high ‘displacement advantage’, permitting more cursorial species to cycle their limbs more quickly) and (ii) longer, more gracile limb bones, particularly at the distal segments (as a means of decreasing rotational inertia). As predicted, highly cursorial jackrabbits are typically marked by the lowest mechanical advantage and the longest distal segments, non‐cursorial pikas display the highest mechanical advantage and the shortest distal segments, and rabbits generally display intermediate values for these variables. Variation in long bone robusticity followed a proximodistal gradient. Whereas proximal limb bone robusticity declined with cursoriality, distal limb bone robusticity generally remained constant across the three species. The association between long, structurally gracile limb bones and decreased maximal bending strength suggests that the more cursorial lagomorphs compromise proximal limb bone integrity to improve locomotor economy. In contrast, the integrity of distal limb bones is maintained with increasing cursoriality, suggesting that the safety factor takes priority over locomotor economy in those regions of the postcranial skeleton that experience higher loading during locomotion. Overall, these findings support the hypothesis that cursoriality is associated with a common suite of morphological adaptations across a range of body sizes and radiations.     

Functional morphology of the muscular sling at the pectoral girdle in tree sloths: convergent morphological solutions to new functional demands?

Recent phylogenetic analyses imply a diphyly of tree sloths and a convergent evolution of their obligatory suspensory locomotion. In mammals the extrinsic shoulder musculature forms a ‘muscular sling’ to support the trunk in quadrupedal postures. In addition, the extrinsic pectoral muscles are responsible for moving the proximal forelimb elements during locomotion. Due to the inverse orientation of the body in regard to the gravitational force, the muscular sling as configured as in pronograde mammals is unsuited to suspend the weight of the thorax in sloths. We here review the muscular topography of the shoulder in Choloepus didactylus and Bradypus variegatus in the light of presumably convergent evolution to adapt to the altered functional demands of the inverse orientation of the body. In addition, we venture to deduce the effect of the shoulder musculature of C. didactylus during locomotion based on previously published 3D kinematic data. Finally, we assess likely convergences in the muscular topography of both extant sloth lineages to test the hypothesis that convergent evolution is reflected by differing morphological solutions to the same functional demands posed by the suspensory posture. Muscular topography of the shoulder in C. didactylus is altered from the plesiomorphic condition of pronograde mammals, whereas the shoulder in B. variegatus more closely resembles the general pattern. Overall kinematics as well as the muscles suitable for pro‐ and retraction of the forelimb were found to be largely comparable to pronograde mammals in C. didactylus. We conclude that most of the peculiar topography of extrinsic forelimb musculature can be attributed to the inverse orientation of the body. These characteristics are often similar in both genera, but we also identified different morphological solutions that evolved to satisfy the new functional demands and are indicative of convergent evolution. We suggest that the shared phylogenetic heritage canalized the spectrum of possible solutions to new functional demands, and digging adaptations of early xenarthrans posed morphological constraints that resulted in similar suspensory postures. The data of this study, including muscle maps, will be helpful to infer locomotor characteristics of fossil sloths.     

The inner ear of Megatherium and the evolution of the vestibular system in sloths

Extant tree sloths are uniquely slow mammals with a very specialized suspensory behavior. To improve our understanding of their peculiar evolution, we investigated the inner ear morphology of one of the largest and most popular fossil ground sloths, Megatherium americanum. We first address the predicted agility of this animal from the scaling of its semicircular canals (SC) relative to body mass, based on recent work that provided evidence that the size of the SC in mammals correlates with body mass and levels of agility. Our analyses predict intermediate levels of agility for Megatherium, contrasting with the extreme slowness of extant sloths. Secondly, we focus on the morphology of the SC at the inner ear scale and investigate the shape and proportions of these structures in Megatherium and in a large diversity of extant xenarthrans represented in our database. Our morphometric analyses demonstrate that the giant ground sloth clearly departs from the SC morphology of both extant sloth genera (Choloepus, Bradypus) and is in some aspects closer to that of armadillos and anteaters. Given the close phylogenetic relationships of Megatherium with the extant genus Choloepus, these results are evidence of substantial homoplasy of the SC anatomy in sloths. This homoplasy most likely corresponds to an outstanding convergent evolution between extant suspensory sloth genera.     

Selection of Behaviors and Segmental Coordination During Larval Locomotion Is Disrupted by Nuclear Polyglutamine Inclusions in a New Drosophila Huntington's Disease–Like Model

Abstract: Huntington's disease is an autosomal dominant neurodegenerative disorder that is caused by abnormal expansion of a polyglutamine tract in the huntingtin protein, resulting in intracellular aggregate formation and neurodegeneration. How neuronal cells are affected by such a polyglutamine tract expansion remains obscure. To dissect the ways in which polyglutamine expansion can cause neural dysfunction, the authors generated Drosophila transgenic strains expressing either a nuclear targeted or cytoplasmic form of pathogenic (NHtt-152Q^NLS, NHtt-152Q), or nonpathogenic (NHtt-18Q^NLS, NHtt-18Q) N-terminal human huntingtin. These proteins were expressed in the dendritic arborization neurons of the larval peripheral nervous system and their effects on neuronal survival, morphology, and larval locomotion were examined. The authors found that NHtt-152Q^NLS larvae had altered dendrite morphology and larval locomotion, whereas NHtt-152Q, NHtt-18Q^NLS, and NHtt-18Q larvae did not. Furthermore, the authors examined the physiological defect underlying this disrupted larval locomotion in detail by recording spontaneous ongoing segmental nerve activity. NHtt-152Q^NLS larvae displayed uncoordinated activity between anterior and posterior segments. Moreover, anterior segments had shorter bursts and longer interburst intervals in NHtt-152Q^NLS larvae than in NHtt-18Q^NLS larvae, whereas posterior segments had longer bursts and shorter interburst intervals. These results suggest that the pathogenic protein disrupts neuron function without inducing cell death, and describe how this dysfunction leads to a locomotor defect. These results also suggest that sensory inputs are necessary for the coordination of anterior and posterior body parts during locomotion. From these analyses the authors show that examination of motor behaviors in the Drosophila larvae is a powerful new model to dissect non–cell-lethal mechanisms of mutant Htt toxicity.     

Effects of a Drd2 deletion mutation on ethanol-induced locomotor stimulation and sensitization suggest a role for epistasis

Interpretation of studies using single gene mutants is complicated by possible epistatic interactions with genetic background. Dopamine D₂ receptor (Drd2) knockout mice on a C57BL/6 (B6) background show decreased basal locomotion, ethanol preference and ethanol-induced ataxia. Epistatic interactions were studied by examining the effect of this null mutation on several traits on a B6 or 129S6 × 129S2 (129) background. Modification of the null mutant effect on ethanol preference by ethanol-induced locomotor sensitization was also examined in B6 background mice. B6 knockout mice exhibited enhanced ethanol-induced locomotor stimulation and sensitization. The reduced ethanol consumption observed in ethanol-naïve B6 Drd2 knockout mice was absent in ethanol-sensitized knockout mice. Ethanol-induced locomotor stimulation was not enhanced in 129 knockout mice, and locomotor sensitization was only modestly increased. However, 129 null mutant mice exhibited reduced basal locomotion and diminished ethanol-induced ataxia, similar to our previous results in B6 mice. The impact of the Drd2 null mutation on a subset of ethanol-related behavioral traits is subject to epistatic influences.     

Muscular Reconstruction and Functional Morphology of the Forelimb of Early Miocene Sloths (Xenarthra,Folivora) of Patagonia

Early Miocene sloths are represented by a diversity of forms ranging from 38 to 95 kg, being registered mainly from Santacrucian Age deposits in southern‐most shores of Patagonia, Argentina. Their postcranial skeleton differs markedly in shape from those of their closest living relatives (arboreal forms of less than 10 kg), Bradypus and Choloepus. In order to gain insight on functional properties of the Santacrucian sloths forelimb, musculature was reconstructed and a comparative, qualitative morphofunctional analysis was performed, allowing proposing hypotheses about biological role of the limb in substrate preferences, and locomotor strategies. The anatomy of the forelimb of Santacrucian sloths resembles more closely extant anteaters such as Tamandua and Myrmecophaga, due to the robustness of the elements, development of features related to attachment of ligaments and muscles, and conservative, pentadactylous, and strong‐clawed manus. The reconstructed forelimb musculature was very well developed and resembles that of extant Pilosa (especially anteaters), although retaining the basic muscular configuration of generalized mammals. This musculature allowed application of powerful forces, especially in adduction of the forelimb, flexion and extension of the antebrachium, and manual prehension. These functional properties are congruent with both climbing and digging activities, and provide support for proposed Santacrucian sloths as good climbing mammals, possibly arboreal or semiarboreal, being also capable diggers. Their climbing strategies were limited, thus these forms relied mainly on great muscular strength and curved claws of the manus to move cautiously on branches. Anat Rec, 2013. © 2012 Wiley Periodicals, Inc.     

Paw Morphology in the Domestic Guinea Pig (Cavia porcellus) and Brown Rat (Rattus norvegicus)

Mammals have adapted to different habitats, food types, and modes of locomotion, which are reflected in a diverse range of paw morphologies. While the behavior of rats and guinea pigs is well defined, especially in terms of their locomotor and foraging behaviors, the anatomy of their foot pads has not yet been explored and compared. This study investigated adaptations in paw morphology in the domestic guinea pig (Cavia porcellus) and the brown rat (Rattus norvegicus). We predicted that rat paws would display adaptations associated with paw dexterity for handling prey items and climbing, whereas guinea pig paws would support mechanical pressure absorption for a herbivorous, sedentary, and terrestrial lifestyle. Using histology techniques and scanning electron microscope, we show that rat paws have many small, deformable pads that are relatively spaced out to enable movement. The pads are clustered toward the anterior of the foot, which coincides with where the most force occurs during locomotion, as rats walk on their toes and toward the front of their paw. Guinea pigs had fewer and larger pads and the posterior pad of the forepaw was textured and contained cartilage, which may act to reduce friction and compression during standing and locomotion. We suggest that differences in paw morphology in rat and guinea pig are associated with loading during locomotion as well as paw mobility. Examining paw morphology and movement abilities in more species will give further insights in to the evolution of locomotor adaptations and paw dexterity in rodents. Anat Rec, 302:2300–2310, 2019. © 2019 American Association for Anatomy     

Inter- and intra-specific scaling of articular surface areas in the hominoid talus

The morphology of postcranial articular surfaces is expected to reflect their weight-bearing properties, as well as the stability and mobility of the articulations to which they contribute. Previous studies have mainly confirmed earlier predictions of isometric scaling between articular surface areas and body mass; the exception to this is 'male-type', convex articular surface areas, which may scale allometrically due to differences in locomotor strategies within the analysed samples. In the present study, we used new surface scanning technology to quantify more accurately articular surface areas and to test those predictions within the talus of hominoid primates, including modern humans. Our results, contrary to predictions, suggest that there are no generalised rules of articular scaling within the talus of hominoids. Instead, we suggest that articular scaling patterns are highly context-specific, depending on the role of each articulation during locomotion, as well as taxon- and sex-specific differences in locomotion and ontogenetic growth trajectories within any given sample. While this may prove problematic for inferring body mass based on articular surface area, it also offers new opportunities of gaining substantial insights into the locomotor patterns of extinct species.     

Exploring the functional morphology of the Gorilla shoulder through musculoskeletal modelling

Musculoskeletal computer models allow us to quantitatively relate morphological features to biomechanical performance. In non-human apes, certain morphological features have long been linked to greater arm abduction potential and increased arm-raising performance, compared to humans. Here, we present the first musculoskeletal model of a western lowland gorilla shoulder to test some of these long-standing proposals. Estimates of moment arms and moments of the glenohumeral abductors (deltoid, supraspinatus and infraspinatus muscles) over arm abduction were conducted for the gorilla model and a previously published human shoulder model. Contrary to previous assumptions, we found that overall glenohumeral abduction potential is similar between Gorilla and Homo. However, gorillas differ by maintaining high abduction moment capacity with the arm raised above horizontal. This difference is linked to a disparity in soft tissue properties, indicating that scapular morphological features like a cranially oriented scapular spine and glenoid do not enhance the abductor function of the gorilla glenohumeral muscles. A functional enhancement due to differences in skeletal morphology was only demonstrated in the gorilla supraspinatus muscle. Contrary to earlier ideas linking a more obliquely oriented scapular spine to greater supraspinatus leverage, our results suggest that increased lateral projection of the greater tubercle of the humerus accounts for the greater biomechanical performance in Gorilla. This study enhances our understanding of the evolution of gorilla locomotion, as well as providing greater insight into the general interaction between anatomy, function and locomotor biomechanics.     

Social grouping tendencies and separation-induced distress in juvenile sheep and goats

Social affinities in juvenile sheep and goats were compared by measuring grouping tendencies and separation-induced distress during experimental encounters with a person in either the presence or the absence of juvenile pen-mates. When tested with pen-mates, sheep spent more time near penmates than did goats. When separated from pen-mates, locomotor activity and plasma corticosteroid titers were higher in sheep, whereas vocal rates were higher in goats. Proximity to pen-mate scores were not correlated with either vocal rates, r = 0.20, or locomotion scores, r = 0.21, recorded when juveniles were tested alone. Proximity to pen-mate scores were correlated with posttest corticosteroid titers, r = 0.70; juvenile sheep spent more time near pen-mates and showed greater adrenocortical responses when temporarily separated from juvenile pen-mates. These findings support the possibility that interspecies differences in emotional reactivity contribute to the differences in grouping tendencies these ungulates display in natural or relatively unrestricted social groups. © 1993 Wiley & sons. Inc.     

The forearm and hand musculature of semi-terrestrial rhesus macaques (Macaca mulatta) and arboreal gibbons (Fam. Hylobatidae). Part I. Description and comparison of the muscle configuration

Primates live in very diverse environments and, as a consequence, show an equally diverse locomotor behaviour. During locomotion, the primate hand interacts with the superstrate and/or substrate and will therefore probably show adaptive signals linked with this locomotor behaviour. Whereas the morphology of the forearm and hand bones have been studied extensively, the functional adaptations in the hand musculature have been documented only scarcely. To evaluate whether there are potential adaptations in forelimb musculature to locomotor behaviour, we investigated the forearm and hand musculature of the highly arboreal gibbons (including Hylobates lar, Hylobates pileatus, Nomascus leucogenys, Nomascus concolor, Symphalangus syndactylus) and compared this with the musculature of the semi-terrestrial rhesus macaques (Macaca mulatta) by performing complete and detailed dissections on a sample of 15 unembalmed specimens. We found that the overall configuration of the upper arm and hand musculature is highly comparable between arboreal gibbons and semi-terrestrial macaques, and follows the general primate condition. Most of the identified differences in muscle configuration are located in the forearm. In macaques, a prominent m. epitrochleoanconeus is present, which potentially helps to extend the forearm and/or stabilize the elbow joint during quadrupedal walking. The m. flexor carpi radialis shows a more radial insertion in gibbons, which might be advantageous during brachiation, as it can aid radial deviation. The fingers of macaques are controlled in pairs by the m. extensor digiti secondi et tertii proprius and the m. extensor digiti quarti et quinti proprius—a similar organization can also be found in their flexors—which might aid in efficient positioning of the hand and fingers on uneven substrates during quadrupedal walking. In contrast, extension of the little finger in gibbons is controlled by a separate m. extensor digiti minimi, whereas digits 2 to 4 are extended by the m. extensor digitorum brevis, suggesting that simultaneous extension of digits 2–4 in gibbons might be important when reaching or grasping an overhead support during brachiation. In conclusion, the overall configuration of the forelimb and hand musculature is very similar in gibbons and macaques, with some peculiarities which can be linked to differences in forelimb function and which might be related to the specific locomotor behaviour of each group.