Gabrielle A. Russo

Evolution of the hominoid vertebral column: The long and the short of it.

The postcranial axial skeleton exhibits considerable morphological and functional diversity among living primates. Particularly striking are the derived features in hominoids that distinguish them from most other primates and mammals. In contrast to the primitive catarrhine morphotype, which presumably possessed an external (protruding) tail and emphasized more pronograde trunk posture, all living hominoids are characterized by the absence of an external tail and adaptations to orthograde trunk posture. Moreover, modern humans evolved unique vertebral features that satisfy the demands of balancing an upright torso over the hind limbs during habitual terrestrial bipedalism. Our ability to identify the evolutionary timing and understand the functional and phylogenetic significance of these fundamental changes in postcranial axial skeletal anatomy in the hominoid fossil record is key to reconstructing ancestral hominoid patterns and retracing the evolutionary pathways that led to living apes and modern humans. Here, we provide an overview of what is known about evolution of the hominoid vertebral column, focusing on the currently available anatomical evidence of three major transitions: tail loss and adaptations to orthograde posture and bipedal locomotion.

Foramen magnum position in bipedal mammals.

The anterior position of the human foramen magnum is often explained as an adaptation for maintaining balance of the head atop the cervical vertebral column during bipedalism and the assumption of orthograde trunk postures. Accordingly, the relative placement of the foramen magnum on the basicranium has been used to infer bipedal locomotion and hominin status for a number of Mio-Pliocene fossil taxa. Nonetheless, previous studies have struggled to validate the functional link between foramen magnum position and bipedal locomotion. Here, we test the hypothesis that an anteriorly positioned foramen magnum is related to bipedalism through a comparison of basicranial anatomy between bipeds and quadrupeds from three mammalian clades: marsupials, rodents and primates. Additionally, we examine whether strepsirrhine primates that habitually assume orthograde trunk postures exhibit more anteriorly positioned foramina magna compared with non-orthograde strepsirrhines. Our comparative data reveal that bipedal marsupials and rodents have foramina magna that are more anteriorly located than those of quadrupedal close relatives. The foramen magnum is also situated more anteriorly in orthograde strepsirrhines than in pronograde or antipronograde strepsirrhines. Among the primates sampled, humans exhibit the most anteriorly positioned foramina magna. The results of this analysis support the utility of foramen magnum position as an indicator of bipedal locomotion in fossil hominins.

Reevaluation of the lumbosacral region of Oreopithecus bambolii.

Functional interpretations of the postcranium of the late Miocene ape Oreopithecus bambolii are controversial. The claim that Oreopithecus practiced habitual terrestrial bipedalism is partly based on restored postcranial remains originally recovered from Baccinello, Tuscany (Köhler and Moyà-Solà, 1997). The lower lumbar vertebrae of BA#72 were cited as evidence that Oreopithecus exhibits features indicative of a lordotic lumbar spine, including dorsal wedging of the vertebral bodies and a caudally progressive increase in postzygapophyseal interfacet distance. Here, we demonstrate why the dorsal wedging index value obtained by Köhler and Moyà-Solà (1997) for the BA#72 last lumbar vertebra is questionable due to distortion in that region, present a more reliable way to measure postzygapophyseal interfacet distance, and include an additional metric (laminar width) with which to examine changes in the transverse dimensions of the neural arches. We also quantify the external morphology of the BA#72 proximal sacrum, which, despite well-documented links between sacral morphology and bipedal locomotion, and excellent preservation of the sacral prezygapophyses, first sacral vertebral body, and right ala, was not evaluated by Köhler and Moyà-Solà (1997). Measures of postzygapophyseal interfacet distance and laminar width on the penultimate and last lumbar vertebrae of BA#72 reveal a pattern encompassed within the range of living nonhuman hominoids and unlike that of modern humans, suggesting that Oreopithecus did not possess a lordotic lumbar spine. Results further show that the BA#72 sacrum exhibits relatively small prezygapophyseal articular facet surface areas and mediolaterally narrow alae compared with modern humans, indicating that the morphology of the Oreopithecus sacrum is incompatible with the functional demands of habitual bipedal stance and locomotion. The Oreopithecus lumbosacral region does not exhibit adaptations for habitual bipedal locomotion.

Tail growth tracks the ontogeny of prehensile tail use in capuchin monkeys (Cebus albifrons and C. apella).

Physical anthropologists have devoted considerable attention to the structure and function of the primate prehensile tail. Nevertheless, previous morphological studies have concentrated solely on adults, despite behavioral evidence that among many primate taxa, including capuchin monkeys, infants and juveniles use their prehensile tails during a greater number and greater variety of positional behaviors than do adults. In this study, we track caudal vertebral growth in a mixed longitudinal sample of white-fronted and brown capuchin monkeys (Cebus albifrons and Cebus apella). We hypothesized that young capuchins would have relatively robust caudal vertebrae, affording them greater tail strength for more frequent tail-suspension behaviors. Our results supported this hypothesis. Caudal vertebral bending strength (measured as polar section modulus at midshaft) scaled to body mass with negative allometry, while craniocaudal length scaled to body mass with positive allometry, indicating that infant and juvenile capuchin monkeys are characterized by particularly strong caudal vertebrae for their body size. These findings complement previous results showing that long bone strength similarly scales with negative ontogenetic allometry in capuchin monkeys and add to a growing body of literature documenting the synergy between postcranial growth and the changing locomotor demands of maturing animals. Although expanded morphometric data on tail growth and behavioral data on locomotor development are required, the results of this study suggest that the adult capuchin prehensile-tail phenotype may be attributable, at least in part, to selection on juvenile performance, a possibility that deserves further attention.

Postsacral Vertebral Morphology in Relation to Tail Length Among Primates and Other Mammals

Tail reduction/loss independently evolved in a number of mammalian lineages, including hominoid primates. One prerequisite to appropriately contextualizing its occurrence and understanding its significance is the ability to track evolutionary changes in tail length throughout the fossil record. However, to date, the bony correlates of tail length variation among living taxa have not been comprehensively examined. This study quantifies postsacral vertebral morphology among living primates and other mammals known to differ in relative tail length (RTL). Linear and angular measurements with known biomechanical significance were collected on the first, mid‐, and transition proximal postsacral vertebrae, and their relationship with RTL was assessed using phylogenetic generalized least‐squares regression methods. Compared to shorter‐tailed primates, longer‐tailed primates possess a greater number of postsacral vertebral features associated with increased proximal tail flexibility (e.g., craniocaudally longer vertebral bodies), increased intervertebral body joint range of motion (e.g., more circularly shaped cranial articular surfaces), and increased leverage of tail musculature (e.g., longer spinous processes). These observations are corroborated by the comparative mammalian sample, which shows that distantly related short‐tailed (e.g., Phascolarctos, Lynx) and long‐tailed (e.g., Dendrolagus, Acinonyx) nonprimate mammals morphologically converge with short‐tailed (e.g., Macaca tonkeana) and long‐tailed (e.g., Macaca fascicularis) primates, respectively. Multivariate models demonstrate that the variables examined account for 70% (all mammals) to 94% (only primates) of the variance in RTL. Results of this study may be used to infer the tail lengths of extinct primates and other mammals, thereby improving our understanding about the evolution of tail reduction/loss. Anat Rec, 298:354–375, 2015.

Another look at the foramen magnum in bipedal mammals

A more anteriorly positioned foramen magnum evolved in concert with bipedalism at least four times within Mammalia: once in macropodid marsupials, once in heteromyid rodents, once in dipodid rodents, and once in hominoid primates. Here, we expand upon previous research on the factors influencing mammalian foramen magnum position (FMP) and angle with four new analyses. First, we quantify FMP using a metric (basioccipital ratio) not previously examined in a broad comparative sample of mammals. Second, we evaluate the potential influence of relative brain size on both FMP and foramen magnum angle (FMA). Third, we assess FMP in an additional rodent clade (Anomaluroidea) containing bipedal springhares (Pedetes spp.) and gliding/quadrupedal anomalures (Anomalurus spp.). Fourth, we determine the relationship between measures of FMP and FMA in extant hominoids and an expanded mammalian sample. Our results indicate that bipedal/orthograde mammals have shorter basioccipitals than their quadrupedal/non-orthograde relatives. Brain size alone has no discernible effect on FMP or FMA. Brain size relative to palate size has a weak influence on FMP in some clades, but effects are not evident in all metrics of FMP and are inconsistent among clades. Among anomaluroids, bipedal Pedetes exhibits a more anterior FMP than gliding/quadrupedal Anomalurus. The relationship between FMA and FMP in hominoids depends on the metric chosen for quantifying FMP, and if modern humans are included in the sample. However, the relationship between FMA and FMP is nonexistent or weak across rodents, marsupials, and, to a lesser extent, strepsirrhine primates. These results provide further evidence that bipedal mammals tend to have more anteriorly positioned foramina magna than their quadrupedal close relatives. Our findings also suggest that the evolution of FMP and FMA in hominins may not be closely coupled.

Tail Function During Arboreal Quadrupedalism in Squirrel Monkeys (Saimiri boliviensis) and Tamarins (Saguinus oedipus)

The need to maintain stability on narrow branches is often presented as a major selective force shaping primate morphology, with adaptations to facilitate grasping receiving particular attention. The functional importance of a long and mobile tail for maintaining arboreal stability has been comparatively understudied. Tails can facilitate arboreal balance by acting as either static counterbalances or dynamic inertial appendages able to modulate whole-body angular momentum. We investigate associations between tail use and inferred grasping ability in two closely related cebid platyrrhines-cotton-top tamarins (Saguinus oedipus) and black-capped squirrel monkeys (Saimiri boliviensis). Using high-speed videography of captive monkeys moving on 3.2 cm diameter poles, we specifically test the hypothesis that squirrel monkeys (characterized by grasping extremities with long digits) will be less dependent on the tail for balance than tamarins (characterized by claw-like nails, short digits, and a reduced hallux). Tamarins have relatively longer tails than squirrel monkeys, move their tails through greater angular amplitudes, at higher angular velocities, and with greater angular accelerations, suggesting dynamic use of tail to regulate whole-body angular momentum. By contrast, squirrel monkeys generally hold their tails in a comparatively stationary posture and at more depressed angles, suggesting a static counterbalancing mechanism. This study, the first empirical test of functional tradeoffs between grasping ability and tail use in arboreal primates, suggests a critical role for the tail in maintaining stability during arboreal quadrupedalism. Our findings have the potential to inform our functional understanding of tail loss during primate evolution.

The fifth element (of Lucy's sacrum): Reply to Machnicki, Lovejoy, and Reno

Last year, we (Russo & Williams, 2015) asserted that the fifth element in the “Lucy” Australopithecus afarensis sacrum (A.L. 288-1an) is damaged but that in several features it is morphologically more similar to a last sacral (LS) vertebra than to a fused first coccygeal (Co1) vertebra. We thus argued that it cannot be touted as an example of a fourelement sacrum in the early hominin fossil record in support of the “long-back” model of hominoid vertebral evolution (McCollum, Rosenman, Suwa, Meindl, & Lovejoy, 2010), which posits that hominins evolved from an ancestor with a long (6–7 element) lumbar column (in contrast to 3–4 lumbar vertebrae and a concomitantly longer sacrum invoked in the “short-back”model). Machnicki, Lovejoy, & Reno (2016) recently challenged our conclusions along several lines, first contending that the fifth segment is minimally damaged and its sacral foramina are not affected by postmortem breakage or distortion. Here, we argue that damage to the fifth element’s lateral (transverse) processes is not insignificant (contra Machnicki et al., 2016; McCollum et al., 2010). In their assessment of A.L. 288-1an, Johanson et al. (1982, p. 436) note that the specimen is “substantially deformed by some degree of crushing, which is exhibited by numerous fossilization cracks and a general deviation of the distal portion to the left of the midline.” Distortion due to crushing, torsion, and possible expanding matrix is apparent throughout the sacrum, resulting in both mediolateral and craniocaudal flattening, the former from ventrally-displaced alae and auricular and retroauricular areas, and the latter from compression along the sacral bodies (see Johanson et al., 1982). As noted by Johanson et al. (1982), the median sacral crest is broken and collapsed into the sacral hiatus at the first and fourth/fifth sacral levels, and the second to fifth elements are skewed to the left (Figure 1A,B). Following the description by Johanson et al. (1982), we have highlighted the extensive cracking, separation, and buckling that appear to have occurred post-deposition (Figure 1C,D). The right ala and dorsal wall are cracked and displaced dorsally, culminating in the separated lateral process at the level of S4 (Figure 1B,D). It is of relevance that Johanson et al. (1982) noted that the left auricular surface and retroauricular region likely suffer from plastic deformation, resulting in a crushed and dorsally rotated aspect of the auricular surface and resultant deepening of the retroauricular fossa and foreshortening of the length of the total auricular surface (Figure 1C,D). Furthermore, they note that “During fossilization, pressure was clearly applied on the sacrum and innominate while still in articulation as the two fit very closely together, but the sacroiliac region of each has been distorted” (p. 423). We have highlighted the dorsolateral crushing evident in the medial aspect of the iliac crest—the posterior superior iliac spine and the entirety of the ilia tuberosity, including the retroauricular area (Figure 1E). Cracks are extensive in this region of the os coxa and spread across the iliac blade. Together, evidence of damage and distortion in the sacrum and os coxa seem consistent with compressive and torsional dorsoventrally-directed stress on the right ala and cranio-lateral pressure on sacral elements 2–5 and the left ala, resulting in buckling of the auricular surfaces and posterior iliac blade. The left lateral process of the fifth element is covered by adhering matrix (contra McCollum et al., 2010) (horizontal arrows, Figure 1A,B; see also Figure 4 in Machnicki et al., 2016), and it is probably broken laterally. It is noteworthy that the bottom of the fourth left lateral process is complete; thus, any now-missing aspect of the fifth left lateral process would not have come in direct contact with that of the fourth. However, as a result of the aforementioned damage, the lateral process extending from S3 to S4 is broken (vertical arrows, Figure 1A,B) and pulled apart on the right side (Figure 1C,D). It is similarly likely that the right lateral processes of the fourth and fifth elements are now positioned further apart from one another than they were in life (Figure 1C,D). While these right lateral processes are complete and not broken, meaning that they were not fused in life, we nevertheless think they would have contributed to a near-complete sacral foramen according to Schultz’s criteria (see figure 5C in Machnicki et al., 2016). Furthermore, it is precisely because the A.L. 288-1an lateral processes are damaged/distorted (and so sacral foramen formation is indeterminate) that we initially proposed a study of alternative morphological approaches—sacral hiatus level, cornua projection, and articular surface shape—to sacro-coccygeal differentiation (Russo & Williams, 2015). Quantification of all three morphologies supported a sacral identity of the terminal element of A.L. 288-1an (Russo & Williams, 2015). Machnicki et al. (2016) focused on the position of the apex of the sacral hiatus, which they argued is highly variable and therefore not a useful

Giant pandas (Carnivora: Ailuropoda melanoleuca) and living hominoids converge on lumbar vertebral adaptations to orthograde trunk posture.

Living hominoids share a common body plan characterized by a gradient of derived postcranial features that distinguish them from their closest living relatives, cercopithecoid monkeys. However, the evolutionary scenario(s) that led to the derived postcranial features of hominoids are uncertain. Explanations are complicated by the fact that living hominoids vary considerably in positional behaviors, and some Miocene hominoids are morphologically, and therefore probably behaviorally, distinct from modern hominoids. Comparative studies that aim to identify morphologies associated with specific components of positional behavioral repertoires are an important avenue of research that can improve our understanding of the evolution and adaptive significance of the hominoid postcranium. Here, we employ a comparative approach to offer additional insight into the evolution of the hominoid lumbar vertebral column. Specifically, we tested whether giant pandas (Carnivora: Ailuropoda melanoleuca) converge with living hominoids on lumbar vertebral adaptations to the single component of their respective positional behavioral repertoires that they share--orthograde (i.e., upright) trunk posture. We compare lumbar vertebral morphologies of Ailuropoda to those of other living ursids and caniform outgroups (northern raccoons and gray wolves). Mirroring known differences between living hominoids and cercopithecoids, Ailuropoda generally exhibits fewer, craniocaudally shorter lumbar vertebrae with more dorsally positioned transverse processes that are more dorsally oriented and laterally directed, and taller, more caudally directed spinous processes than other caniforms in the sample. Our comparative evidence lends support to a potential evolutionary scenario in which the acquisition of hominoid-like lumbar vertebral morphologies may have evolved for generalized orthograde behaviors and could have been exapted for suspensory behavior in crown hominoids and for other locomotor specializations (e.g., brachiation) in extant lineages.

Trabecular bone structural variation in the proximal sacrum among primates: Trabecular bone structure in the primate sacrum

The sacrum occupies a functionally important anatomical position as part of the pelvic girdle and vertebral column. Sacral orientation and external morphology in modern humans are distinct from those in other primates and compatible with the demands of habitual bipedal locomotion. Among nonhuman primates, however, how sacral anatomy relates to positional behaviors is less clear. As an alternative to evaluation of the sacrums external morphology, this study assesses if the sacrums internal morphology (i.e., trabecular bone) differs among extant primates. The primary hypothesis tested is that trabecular bone parameters with established functional relevance will differ in the first sacral vertebra (S1) among extant primates that vary in positional behaviors. Results for analyses of individual variables demonstrate that bone volume fraction, degree of anisotropy, trabecular number, and size‐corrected trabecular thickness differ among primates grouped by positional behaviors to some extent, but not always in ways consistent with functional expectations. When examined as a suite, these trabecular parameters distinguish obligate bipeds from other positional behavior groups; and, the latter three trabecular bone variables further distinguish knuckle‐walking terrestrial quadrupeds from manual suspensor‐brachiators, vertical clingers and leapers, and arboreal quadrupeds, as well as between arboreal and terrestrial quadrupeds. As in other regions of the skeleton in modern humans, trabecular bone in S1 exhibits distinctively low bone volume fraction. Results from this study of extant primate S1 trabecular bone structural variation provide a functional context for interpretations concerning the positional behaviors of extinct primates based on internal sacral morphology. Anat Rec, 302:1354–1371, 2019.