Hedonic eating, obesity, and addiction result from increased neuropeptide Y in the nucleus accumbens during human brain evolution.

The nucleus accumbens (NAc) is central to motivation and action, exhibiting one of the highest densities of neuropeptide Y (NPY) in the brain. Within the NAc, NPY plays a role in reward and is involved in emotional behavior and in increasing alcohol and drug addiction and fat intake. Here, we examined NPY innervation and neurons of the NAc in humans and other anthropoid primates in order to determine whether there are differences among these various species that would correspond to behavioral or life history variables. We quantified NPY-immunoreactive axons and neurons in the NAc of 13 primate species, including humans, great apes, and monkeys. Our data show that the human brain is unique among primates in having denser NPY innervation within the NAc, as measured by axon length density to neuron density, even after accounting for brain size. Combined with our previous finding of increased dopaminergic innervation in the same region, our results suggest that the neurochemical profile of the human NAc appears to have rendered our species uniquely susceptible to neurophysiological conditions such as addiction. The increase in NPY specific to the NAc may represent an adaptation that favors fat intake and contributes to an increased vulnerability to eating disorders, obesity, as well as alcohol and drug dependence. Along with our findings for dopamine, these deeply rooted structural attributes of the human brain are likely to have emerged early in the human clade, laying the groundwork for later brain expansion and the development of cognitive and behavioral specializations.

The hominid ilium is shaped by a synapomorphic growth mechanism that is unique within primates.

The human ilium is significantly shorter and broader than those of all other primates. In addition, it exhibits an anterior inferior iliac spine (AIIS) that emerges via a secondary center of ossification, which is unique to hominids (i.e., all taxa related to the human clade following their phyletic separation from the African apes). Here, we track the ontogeny of human and other primate ossa coxae. The human pattern is unique, from anlage to adulthood, and fusion of its AIIS is the capstone event in a repositioning of the anterior gluteals that maximizes control of pelvic drop during upright walking. It is therefore a hominid synapomorphy that can be used to assess the presence and age of bipedal locomotion in extinct taxa.

Early hominids may have been weed species.

Panid, gorillid, and hominid social structures appear to have diverged as dramatically as did their locomotor patterns as they emerged from a late Miocene last common ancestor (LCA). Despite their elimination of the sectorial canine complex and adoption of bipedality with its attendant removal of their ready access to the arboreal canopy, Australopithecus was able to easily invade novel habitats after florescence from its likely ancestral genus, Ardipithecus sp. Other hominoids, unable to sustain sufficient population growth, began an inexorable decline, culminating in their restriction to modern refugia. Success similar to that of earliest hominids also characterizes several species of macaques, often termed "weed species." We here review their most salient demographic features and find that a key element is irregularly elevated female survival. It is reasonable to conclude that a similar feature characterized early hominids, most likely made possible by the adoption of social monogamy. Reduced female mortality is a more probable key to early hominid success than a reduction in birth space, which would have been physiologically more difficult.

A neurochemical hypothesis for the origin of hominids.

It has always been difficult to account for the evolution of certain human characters such as language, empathy, and altruism via individual reproductive success. However, the striatum, a subcortical region originally thought to be exclusively motor, is now known to contribute to social behaviors and "personality styles" that may link such complexities with natural selection. We here report that the human striatum exhibits a unique neurochemical profile that differs dramatically from those of other primates. The human signature of elevated striatal dopamine, serotonin, and neuropeptide Y, coupled with lowered acetylcholine, systematically favors externally driven behavior and greatly amplifies sensitivity to social cues that promote social conformity, empathy, and altruism. We propose that selection induced an initial form of this profile in early hominids, which increased their affiliative behavior, and that this shift either preceded or accompanied the adoption of bipedality and elimination of the sectorial canine. We further hypothesize that these changes were critical for increased individual fitness and promoted the adoption of social monogamy, which progressively increased cooperation as well as a dependence on tradition-based cultural transmission. These eventually facilitated the acquisition of language by elevating the reproductive advantage afforded those most sensitive to social cues.

Odd-nosed monkey scapular morphology converges on that of arm-swinging apes.

Odd-nosed monkeys 'arm-swing' more frequently than other colobines. They are therefore somewhat behaviorally analogous to atelines and apes. Scapular morphology regularly reflects locomotor mode, with both arm-swinging and climbing anthropoids showing similar characteristics, especially a mediolaterally narrow blade and cranially angled spine and glenoid. However, these traits are not expressed uniformly among anthropoids. Therefore, behavioral convergences in the odd-nosed taxa of Nasalis, Pygathrix, and Rhinopithecus with hominoids may not have resulted in similar structural convergences. We therefore used a broad sample of anthropoids to test how closely odd-nosed monkey scapulae resemble those of other arm-swinging primates. We used principal component analyses on size-corrected linear metrics and angles that reflect scapular size and shape in a broad sample of anthropoids. As in previous studies, our first component separated terrestrial and above-branch quadrupeds from clambering and arm-swinging taxa. On this axis, odd-nosed monkeys were closer than other colobines to modern apes and Ateles. All three odd-nosed genera retain glenoid orientations that are more typical of other colobines, but Pygathrix and Rhinopithecus are closer to hominoids than to other Asian colobines in mediolateral blade breadth, spine angle, and glenoid position. This suggests that scapular morphology of Pygathrix may reflect a significant reliance on arm-swinging and that the morphology of Rhinopithecus may reflect more reliance on general climbing. As 'arm-swinging' features are also found in taxa that only rarely arm-swing, we hypothesize that these features are also adaptive for scrambling and bridging in larger bodied anthropoids that use the fine-branch component of their arboreal niches.

Neither chimpanzee nor human, Ardipithecus reveals the surprising ancestry of both.

Australopithecus fossils were regularly interpreted during the late 20th century in a framework that used living African apes, especially chimpanzees, as proxies for the immediate ancestors of the human clade. Such projection is now largely nullified by the discovery of Ardipithecus. In the context of accumulating evidence from genetics, developmental biology, anatomy, ecology, biogeography, and geology, Ardipithecus alters perspectives on how our earliest hominid ancestors--and our closest living relatives--evolved.

Evolution of the hominoid scapula and its implications for earliest hominid locomotion.

OBJECTIVES: The higher primate scapula has been subject to many explanations of the putative "adaptive value" of its individual traits. However, the shift from the bone's position in above branch quadrupeds to its more posterolateral position in recent hominoids obviously required fundamental changes to its general form. We hypothesize that most features argued to be individually adaptive are more likely secondary consequences of changes in its fundamental bauplan, a view more consistent with modern developmental biology. MATERIALS AND METHODS: We tested this hypothesis with scapular metrics and angles from a broad anthropoid sample. RESULTS: Our results support our hypothesis. Contrary to earlier predictions, vertebral border length differs little relative to body size in anthropoids, inferior angle position primarily reflects mediolateral scapular breadth, and supraspinous and infraspinous fossa sizes largely reflect scapular spine orientation. Suspensory taxa have cranially oriented glenoids, whereas slow clamberers and humans do not. Australopithecus most closely resembles the latter. DISCUSSION: Most scapular features can be explained by only two primary changes: (1) reduction in mediolateral breadth and (2) change in the glenoid position relative to the vertebral border with increased reliance on suspension, which led to a more cranially angled scapular spine. Virtually all other scapular traits appear to be byproducts of these two changes. Based on fossil morphology, hominids1 were derived from a last common ancestor primarily adapted for clambering and not for suspension. Scapular form in early hominids such as Australopithecus is therefore primitive and largely reflects the genus's general clambering heritage.

Anterolateral ligament anatomy: a comparative anatomical study.

PURPOSE: Some anatomical studies have indicated that the anterolateral ligament (ALL) of the knee is distinct ligamentous structure in humans. The purpose of this study is to compare the lateral anatomy of the knee among human and various animal specimens. METHODS: Fifty-eight fresh-frozen knee specimens, from 24 different animal species, were used for this anatomical study. The same researchers dissected all the specimens in this study, and dissections were performed in a careful and standardized manner. RESULTS: An ALL was not found in any of the 58 knees dissected. Another interesting finding in this study is that some primate species (the prosimians: the red and black and white lemurs) have two LCLs. CONCLUSION: The clinical relevance of this study is the lack of isolation of the ALL as a unique structure in animal species. Therefore, precaution is recommended before assessing the need for surgery to reconstruct the ALL as a singular ligament.

Locomotor pattern fails to predict foramen magnum angle in rodents, strepsirrhine primates, and marsupials.

Foramen magnum position has traditionally been used as an indicator of bipedality because it has been thought to favor a more "balanced" skull position. Here, we analyzed foramen magnum angle (FMA) in relation to locomotion in three mammalian orders that include bipedal or orthograde species in addition to quadrupedal or pronograde species. In marsupials and strepsirrhine primates, we found that there is no relationship between locomotor pattern and FMA. In rodents, we found that there is a significant difference in FMA between bipedal and quadrupedal rodents. However, when these species are analyzed in the context of enlarged auditory bullae, this relationship is no longer significant. Additionally, we find a significant relationship between relative brain size and FMA in strepsirrhine primates. Taken together, these data indicate that several developmental modules of the cranium influence FMA, but that locomotion does not. We caution that basicranial evolution is a complex phenomenon that must be explored in the context of each taxon's unique evolutionary and developmental history.

Developmental identity versus typology: Lucy has only four sacral segments.

OBJECTIVES: Both interspecific and intraspecific variation in vertebral counts reflect the action of patterning control mechanisms such as Hox. The preserved A.L. 288-1 ("Lucy") sacrum contains five fused elements. However, the transverse processes of the most caudal element do not contact those of the segment immediately craniad to it, leaving incomplete sacral foramina on both sides. This conforms to the traditional definition of four-segmented sacra, which are very rare in humans and African apes. It was recently suggested that fossilization damage precludes interpretation of this specimen and that additional sacral-like features of its last segment (e.g., the extent of the sacral hiatus) suggest a general Australopithecus pattern of five sacral vertebrae. METHODS: We provide updated descriptions of the original Lucy sacrum. We evaluate sacral/coccygeal variation in a large sample of extant hominoids and place it within the context of developmental variation in the mammalian vertebral column. RESULTS: We report that fossilization damage did not shorten the transverse processes of the fifth segment of Lucy's sacrum. In addition, we find that the extent of the sacral hiatus is too variable in apes and hominids to provide meaningful information on segment identity. Most importantly, a combination of sacral and coccygeal features is to be expected in vertebrae at regional boundaries. DISCUSSION: The sacral/caudal boundary appears to be displaced cranially in early hominids relative to extant African apes and humans, a condition consistent with the likely ancestral condition for Miocene hominoids. While not definitive in itself, a four-segmented sacrum accords well with the "long-back" model for the Pan/Homo last common ancestor. Am J Phys Anthropol 160:729-739, 2016. © 2016 Wiley Periodicals, Inc.

Let bone and muscle talk together: a study of real and virtual dissection and its implications for femoral musculoskeletal structure of chimpanzees.

Proximal femoral morphology and associated musculature are of special relevance to the understanding of hominoid locomotor systems. Knowledge of bone-muscle correspondence in extant hominoids forms an important comparative basis for inferring structure-function relationships in fossil hominids. However, there is still a lack of consensus on the correspondence between muscle attachment sites and surface morphology of the proximal femoral diaphysis in chimpanzees. Two alternative observations have been proposed regarding the attachment site positions of gluteus maximus (GM) and vastus lateralis (VL) relative to two prominent surface features of the proximal femoral diaphysis, the lateral spiral pilaster and the inferolateral fossa. Here, we use a combination of virtual and physical dissection in an attempt to identify the exact correspondence between muscle attachment sites and osteological features in two specimens of Pan troglodytes verus. The results show that the insertion of the GM tendon is consistently inferolateral to the lateral spiral pilaster, and that a part of the inferolateral fossa consistently forms the attachment site of the VL muscular fibers. While overall musculoskeletal features are similar in the two specimens examined in this study, GM and VL exhibit different degrees of segregation at the level of the inferolateral fossa. One specimen exhibited tendinous GM fibers penetrating the posteromedial part of VL, with both GM and VL inserting at the inferolateral fossa. In the other specimen, GM and VL were separated by a lateral intermuscular septum, which inserted into the inferolateral fossa. Variation of proximal femoral muscle attachments in chimpanzees is thus greater than previously thought. Our results indicate that a conspicuous osteological feature such as the inferolateral fossa does not necessarily correspond to the attachment site of a single muscle, but could serve as a boundary region between two muscles. Caution is thus warranted when interpreting the surface topography of muscle attachment sites and inferring locomotor functions.

The pisiform growth plate is lost in humans and supports a role for Hox in growth plate formation.

The human pisiform is a small, nodular, although functionally significant, bone of the wrist. In most other mammals, including apes and Australopithecus afarensis, pisiforms are elongate. An underappreciated fact is that the typical mammalian pisiform forms from two ossification centers. We hypothesize that: (i) the presence of a secondary ossification center in mammalian pisiforms indicates the existence of a growth plate; and (ii) human pisiform reduction results from growth plate loss. To address these hypotheses, we surveyed African ape pisiform ossification and confirmed the presence of a late-forming secondary ossification center in chimpanzees and gorillas. Identification of the initial ossification center occurs substantially earlier in apes relative to humans, raising questions concerning the homology of the human pisiform and the two mammalian ossification centers. Second, we conducted histological and immunohistochemical analyses of pisiform ossification in mice. We confirm the presence of two ossification centers separated by organized columnar and hypertrophic chondrocyte zones. Flattened chondrocytes were highly mitotic, indicating the presence of a growth plate. Hox genes have been proposed to play a fundamental role in growth plate patterning. The existence of a pisiform growth plate presents an interesting test case for the association between Hox expression and growth plate formation, and could explain the severe effects on the pisiform observed in Hoxa11 and Hoxd11 knockout mice. Consistent with this hypothesis, we show that Hoxd11 is expressed adjacent to the pisiform in late-stage embryonic mouse limbs supporting a role for Hox genes in growth plate specification. This raises questions concerning the mechanisms regulating Hox expression in the developing carpus.

Metapodial or phalanx? An evolutionary and developmental perspective on the homology of the first ray's proximal segment.

The first mammalian metapodial (MP1) has periodically been argued to actually be a phalanx, because the first ray has one less element than the four posterior rays, and because the MP1 growth plate is proximal like those of all phalanges, rather than distal as in metapodials 2-5. However, growth plates are formed at both ends in non-therian tetrapod metapodials, and phylogenetic analysis demonstrates that growth plate loss is a therian synapomorphy that postdates the establishment of the mammalian phalangeal formula. These data, along with results of developmental and morphological studies, suggest that the MP1 is not a phalanx. The singular, proximal growth plates in MPs 2-5 are likely to be an adaptation to dynamic erect quadrupedal gait which was characterized by conversion of the posterior metapodials into rigid struts with the carpus/tarsus. While the adaptive significance of the reversed ossification of MP1 is less clear, we present three functional/developmental hypotheses.

An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia.

Only one partial skeleton that includes both forelimb and hindlimb elements has been reported for Australopithecus afarensis. The diminutive size of this specimen (A.L. 288-1 ["Lucy"]) has hampered our understanding of the paleobiology of this species absent the potential impact of allometry. Here we describe a large-bodied (i.e., well within the range of living Homo) specimen that, at 3.58 Ma, also substantially antedates A.L. 288-1. It provides fundamental evidence of limb proportions, thoracic form, and locomotor heritage in Australopithecus afarensis. Together, these characteristics further establish that bipedality in Australopithecus was highly evolved and that thoracic form differed substantially from that of either extant African ape.

Asa Issie, Aramis and the origin of Australopithecus.

The origin of Australopithecus, the genus widely interpreted as ancestral to Homo, is a central problem in human evolutionary studies. Australopithecus species differ markedly from extant African apes and candidate ancestral hominids such as Ardipithecus, Orrorin and Sahelanthropus. The earliest described Australopithecus species is Au. anamensis, the probable chronospecies ancestor of Au. afarensis. Here we describe newly discovered fossils from the Middle Awash study area that extend the known Au. anamensis range into northeastern Ethiopia. The new fossils are from chronometrically controlled stratigraphic sequences and date to about 4.1-4.2 million years ago. They include diagnostic craniodental remains, the largest hominid canine yet recovered, and the earliest Australopithecus femur. These new fossils are sampled from a woodland context. Temporal and anatomical intermediacy between Ar. ramidus and Au. afarensis suggest a relatively rapid shift from Ardipithecus to Australopithecus in this region of Africa, involving either replacement or accelerated phyletic evolution.

Temperature regulates limb length in homeotherms by directly modulating cartilage growth.

Allen's Rule documents a century-old biological observation that strong positive correlations exist among latitude, ambient temperature, and limb length in mammals. Although genetic selection for thermoregulatory adaptation is frequently presumed to be the primary basis of this phenomenon, important but frequently overlooked research has shown that appendage outgrowth is also markedly influenced by environmental temperature. Alteration of limb blood flow via vasoconstriction/vasodilation is the current default hypothesis for this growth plasticity, but here we show that tissue perfusion does not fully account for differences in extremity elongation in mice. We show that peripheral tissue temperature closely reflects housing temperature in vivo, and we demonstrate that chondrocyte proliferation and extracellular matrix volume strongly correlate with tissue temperature in metatarsals cultured without vasculature in vitro. Taken together, these data suggest that vasomotor changes likely modulate extremity growth indirectly, via their effects on appendage temperature, rather than vascular nutrient delivery. When combined with classic evolutionary theory, especially genetic assimilation, these results provide a potentially comprehensive explanation of Allen's Rule, and may substantially impact our understanding of phenotypic variation in living and extinct mammals, including humans.

Upright walking has driven unique vascular specialization of the hominin ilium.

BACKGROUND: A novel physis in hominins modulates broadening and shortening of the ilium. We report analysis of a vascular canal system whose origin may be associated with this physis and which appears to be also unique to hominins. Its presence is potentially identifiable in the fossil record by its association with a highly enlarged foramen that is consistently present in modern humans and hominin fossils. METHODS: We measured the diameter of this foramen in humans, fossil hominins, and African great apes and corrected for body size. RESULTS: The mean relative human foramen diameter is significantly greater than those of either Pan or Gorilla. Moreover, eight of the nine values of the Cohen's d for these differences in ratios are highly significant and support the ordering of magnitudes: Pan < Gorilla < Homo. The relative foramen diameter of A.L. 288-1 is above the 75th percentile of all other hominoids and at the high end of humans. The foramen is also present in ARA-VP-6/500. CONCLUSIONS: We posit that the presence and significant enlargement of this foramen in fossils can reasonably serve as an indicator that its anterior inferior iliac spine emerged via the unique hominin physis. The foramen can therefore serve as an indicator of hominin iliac ontogenetic specialization for bipedality in fossil taxa.

The nucleus accumbens and ventral pallidum exhibit greater dopaminergic innervation in humans compared to other primates.

Recent evidence suggests that increased dopaminergic signaling within the dorsal striatum played a central role in the evolution of the human brain. This increase has been linked to human prosociality and language in what has been described as a dopamine-dominated striatum personality style. Increased striatal dopamine is associated with an increase in ventral striatal activity and promotes externally driven behaviors, including cooperation and social conformity. In contrast, decreased striatal dopamine is associated with increased dorsal striatal activity and favors internally driven and goal-oriented behaviors. Previous comparative studies have focused on the dorsal striatum, measuring dopaminergic innervation in the dorsal and medial caudate nucleus and putamen. Here, we add to this knowledge by examining regions of the ventral striatum. We quantified the density of tyrosine hydroxylase-immunoreactive axons, as a measure of dopaminergic innervation, in the nucleus accumbens and ventral pallidum of humans, great apes, platyrrhine and cercopithecid monkeys. Our data show that humans have a significantly greater dopaminergic innervation in both structures, supporting the hypothesis that selection for a prosocial neurochemistry in the human basal ganglia may have contributed to the evolution of our uniquely social behavior profile.