Phylogenetic reduction of the magnocellular red nucleus in primates and inter-subject variability in humans.

Introduction: The red nucleus is part of the motor system controlling limb movements. While this seems to be a function common in many vertebrates, its organization and circuitry have undergone massive changes during evolution. In primates, it is sub-divided into the magnocellular and parvocellular parts that give rise to rubrospinal and rubro-olivary connection, respectively. These two subdivisions are subject to striking variation within the primates and the size of the magnocellular part is markedly reduced in bipedal primates including humans. The parvocellular part is part of the olivo-cerebellar circuitry that is prominent in humans. Despite the well-described differences between species in the literature, systematic comparative studies of the red nucleus remain rare. Methods: We therefore mapped the red nucleus in cytoarchitectonic sections of 20 primate species belonging to 5 primate groups including prosimians, new world monkeys, old world monkeys, non-human apes and humans. We used Ornstein-Uhlenbeck modelling, ancestral state estimation and phylogenetic analysis of covariance to scrutinize the phylogenetic relations of the red nucleus volume. Results: We created openly available high-resolution cytoarchitectonic delineations of the human red nucleus in the microscopic BigBrain model and human probabilistic maps that capture inter-subject variations in quantitative terms. Further, we compared the volume of the nucleus across primates and showed that the parvocellular subdivision scaled proportionally to the brain volume across the groups while the magnocellular part deviated significantly from the scaling in humans and non-human apes. These two groups showed the lowest size of the magnocellular red nucleus relative to the whole brain volume and the largest relative difference between the parvocellular and magnocellular subdivision. Discussion: That is, the red nucleus has transformed from a magnocellular-dominated to a parvocellular-dominated station. It is reasonable to assume that these changes are intertwined with evolutionary developments in other brain regions, in particular the motor system. We speculate that the interspecies variations might partly reflect the differences in hand dexterity but also the tentative involvement of the red nucleus in sensory and cognitive functions.

The evolution of human altriciality and brain development in comparative context.

Human newborns are considered altricial compared with other primates because they are relatively underdeveloped at birth. However, in a broader comparative context, other mammals are more altricial than humans. It has been proposed that altricial development evolved secondarily in humans due to obstetrical or metabolic constraints, and in association with increased brain plasticity. To explore this association, we used comparative data from 140 placental mammals to measure how altriciality evolved in humans and other species. We also estimated how changes in brain size and gestation length influenced the timing of neurodevelopment during hominin evolution. Based on our data, humans show the highest evolutionary rate to become more altricial (measured as the proportion of adult brain size at birth) across all placental mammals, but this results primarily from the pronounced postnatal enlargement of brain size rather than neonatal changes. In addition, we show that only a small number of neurodevelopmental events were shifted to the postnatal period during hominin evolution, and that they were primarily related to the myelination of certain brain pathways. These results indicate that the perception of human altriciality is mostly driven by postnatal changes, and they point to a possible association between the timing of myelination and human neuroplasticity.

Evolutionary scaling and cognitive correlates of primate frontal cortex microstructure.

Investigating evolutionary changes in frontal cortex microstructure is crucial to understanding how modifications of neuron and axon distributions contribute to phylogenetic variation in cognition. In the present study, we characterized microstructural components of dorsolateral prefrontal cortex, orbitofrontal cortex, and primary motor cortex from 14 primate species using measurements of neuropil fraction and immunohistochemical markers for fast-spiking inhibitory interneurons, large pyramidal projection neuron subtypes, serotonergic innervation, and dopaminergic innervation. Results revealed that the rate of evolutionary change was similar across these microstructural variables, except for neuropil fraction, which evolves more slowly and displays the strongest correlation with brain size. We also found that neuropil fraction in orbitofrontal cortex layers V-VI was associated with cross-species variation in performance on experimental tasks that measure self-control. These findings provide insight into the evolutionary reorganization of the primate frontal cortex in relation to brain size scaling and its association with cognitive processes.

A common mechanism drives the alignment between the micro- and macroevolution of primate molars.

A central challenge for biology is to reveal how different levels of biological variation interact and shape diversity. However, recent experimental studies have indicated that prevailing models of evolution cannot readily explain the link between micro- and macroevolution at deep timescales. Here, we suggest that this paradox could be the result of a common mechanism driving a correlated pattern of evolution. We examine the proportionality between genetic variance and patterns of trait evolution in a system whose developmental processes are well understood to gain insight into how such alignment between morphological divergence and genetic variation might be maintained over macroevolutionary time. Primate molars present a model system by which to link developmental processes to evolutionary dynamics because of the biased pattern of variation that results from the developmental architecture regulating their formation. We consider how this biased variation is expressed at the population level, and how it manifests through evolution across primates. There is a strong correspondence between the macroevolutionary rates of primate molar divergence and their genetic variation. This suggests a model of evolution in which selection is closely aligned with the direction of genetic variance, phenotypic variance, and the underlying developmental architecture of anatomical traits.

Not like night and day: the nocturnal letter-winged kite does not differ from diurnal congeners in orbit or endocast morphology.

Nocturnal birds display diverse adaptations of the visual system to low-light conditions. The skulls of birds reflect many of these and are used increasingly to infer nocturnality in extinct species. However, it is unclear how reliable such assessments are, particularly in cases of recent evolutionary transitions to nocturnality. Here, we investigate a case of recently evolved nocturnality in the world's only nocturnal hawk, the letter-winged kite Elanus scriptus. We employed phylogenetically informed analyses of orbit, optic foramen and endocast measurements from three-dimensional reconstructions of micro-computed tomography scanned skulls of the letter-winged kite, two congeners, and 13 other accipitrid and falconid raptors. Contrary to earlier suggestions, the letter-winged kite was not unique in any of our metrics. However, all species of Elanus have significantly higher ratios of orbit versus optic foramen diameter, suggesting high visual sensitivity at the expense of acuity. In addition, visual system morphology varies greatly across accipitrid species, likely reflecting hunting styles. Overall, our results suggest that the transition to nocturnality can occur rapidly and without changes to key hard-tissue indicators of vision, but also that hard-tissue anatomy of the visual system may provide a means of inferring a range of raptor behaviours, well beyond nocturnality.

Unexpected bite-force conservatism as a stable performance foundation across mesoeucrocodylian historical diversity.

Effective interpretation of historical selective regimes requires comprehensive in vivo performance evaluations and well-constrained ecomorphological proxies. The feeding apparatus is a frequent target of such evolutionary studies due to a direct relationship between feeding and survivorship, and the durability of craniodental elements in the fossil record. Among vertebrates, behaviors such as bite force have been central to evaluation of clade dynamics; yet, in the absence of detailed performance studies, such evaluations can misidentify potential selective factors and their roles. Here, we combine the results of a total-clade performance study with fossil-inclusive, phylogenetically informed methods to assess bite-force proxies throughout mesoeucrocodylian evolution. Although bite-force shifts were previously thought to respond to changing rostrodental selective regimes, we find body-size dependent conservation of performance proxies throughout the history of the clade, indicating stabilizing selection for bite-force potential. Such stasis reveals that mesoeucrocodylians with dietary ecologies as disparate as herbivory and hypercarnivory maintain similar bite-force-to-body-size relationships, a pattern which contrasts the precept that vertebrate bite forces should vary most strongly by diet. Furthermore, it may signal that bite-force conservation supported mesoeucrocodylian craniodental disparity by providing a stable performance foundation for the exploration of novel ecomorphospace.

The effect of data provenance on estimates of gestation length in African and Asian colobines.

OBJECTIVES: It seems to be commonly accepted that gestation length within the subfamily Colobinae lasts several weeks longer in the African tribe (Colobini) than in the Asian tribe (Presbytini) even though closely related taxa of similar body mass should have similar life histories. Suspecting problems with data provenance to cause the difference, we revisited the published records expecting similar gestation lengths in both tribes if based on vetted, accurate data. MATERIALS AND METHODS: We compiled published gestation length data for Colobini and Presbytini, labeling them as "unspecified" (n = 16) if the primary reference could not be located, methods were not described, and/or conceptions, the beginning of gestation, were determined based on sporadic observations of mating. If conceptions were determined based on changing hormone levels or patterns of daily mating records, we labeled the data as "accurate" (n = 12). We analyzed the ln transformed data in a phylogenetic framework in relation to adult female body mass. RESULTS: In the unspecified dataset, gestation length in the two tribes overlapped extensively and did not differ significantly. However, in the accurate dataset, gestation length was significantly shorter in Colobini (not longer, as previously assumed). DISCUSSION: Data provenance had a strong impact on the comparison, reversing the relationship in gestation length in the two sister tribes. It remains to be determined why gestation lengths differ, whether, relative to the other primates, Colobini have a shortened gestation or Presbytini a lengthened gestation, and whether similar differences exist in other closely related taxa. Addressing these questions will require additional, broader, comparative analyses.

Rapid evolution of the primate larynx?

Tissue vibrations in the larynx produce most sounds that comprise vocal communication in mammals. Larynx morphology is thus predicted to be a key target for selection, particularly in species with highly developed vocal communication systems. Here, we present a novel database of digitally modeled scanned larynges from 55 different mammalian species, representing a wide range of body sizes in the primate and carnivoran orders. Using phylogenetic comparative methods, we demonstrate that the primate larynx has evolved more rapidly than the carnivoran larynx, resulting in a pattern of larger size and increased deviation from expected allometry with body size. These results imply fundamental differences between primates and carnivorans in the balance of selective forces that constrain larynx size and highlight an evolutionary flexibility in primates that may help explain why we have developed complex and diverse uses of the vocal organ for communication.

Invariant Synapse Density and Neuronal Connectivity Scaling in Primate Neocortical Evolution.

Synapses are involved in the communication of information from one neuron to another. However, a systematic analysis of synapse density in the neocortex from a diversity of species is lacking, limiting what can be understood about the evolution of this fundamental aspect of brain structure. To address this, we quantified synapse density in supragranular layers II-III and infragranular layers V-VI from primary visual cortex and inferior temporal cortex in a sample of 25 species of primates, including humans. We found that synapse densities were relatively constant across these levels of the cortical visual processing hierarchy and did not significantly differ with brain mass, varying by only 1.9-fold across species. We also found that neuron densities decreased in relation to brain enlargement. Consequently, these data show that the number of synapses per neuron significantly rises as a function of brain expansion in these neocortical areas of primates. Humans displayed the highest number of synapses per neuron, but these values were generally within expectations based on brain size. The metabolic and biophysical constraints that regulate uniformity of synapse density, therefore, likely underlie a key principle of neuronal connectivity scaling in primate neocortical evolution.

Costly teeth? Gestation length in primates suggests that neonate dentition is not expensive to produce.

Variation in the relationship between gestation length and body mass can arise because different types of tissue require varying amounts of energy to build, and not all species build such tissues in the same proportions. Given that a pregnant female has a finite amount of energy, trade-offs between investment in different tissues may occur. Here we examine if dental precocity accounts for variation in primate gestation length. If true, this could explain why folivorous species with precocial dentition have longer gestation lengths than predicted by neonatal brain and body mass. We compiled data on gestation length, neonate and adult female body and brain mass from the literature. We used published postcanine eruption schedules at 4 months of age and measured the total occlusal area as dental endowment to approximate dental precocity at birth. Species with embryonic delay in growth or altricial neonates were not considered because they represent grade shifts regarding gestation length. Consequently, our data were biased toward Simiiformes and Old World monkeys, specifically. We performed a phylogenetic generalized least squares regression (pGLS) of neonate brain mass in relation to neonate body mass, and a second pGLS with dental endowment as an additional predictor variable. Including dental endowment in the pGLS did not improve the model. Dental endowment did not systematically impact primate gestation length. Concordant with results from previous studies, this indicates that the energetically expensive period of tooth mineralization may occur postnatally. More data are required to examine if the results are typical across primates.

Tempo and Pattern of Avian Brain Size Evolution.

Relative brain sizes in birds can rival those of primates, but large-scale patterns and drivers of avian brain evolution remain elusive. Here, we explore the evolution of the fundamental brain-body scaling relationship across the origin and evolution of birds. Using a comprehensive dataset sampling> 2,000 modern birds, fossil birds, and theropod dinosaurs, we infer patterns of brain-body co-variation in deep time. Our study confirms that no significant increase in relative brain size accompanied the trend toward miniaturization or evolution of flight during the theropod-bird transition. Critically, however, theropods and basal birds show weaker integration between brain size and body size, allowing for rapid changes in the brain-body relationship that set the stage for dramatic shifts in early crown birds. We infer that major shifts occurred rapidly in the aftermath of the Cretaceous-Paleogene mass extinction within Neoaves, in which multiple clades achieved higher relative brain sizes because of a reduction in body size. Parrots and corvids achieved the largest brains observed in birds via markedly different patterns. Parrots primarily reduced their body size, whereas corvids increased body and brain size simultaneously (with rates of brain size evolution outpacing rates of body size evolution). Collectively, these patterns suggest that an early adaptive radiation in brain size laid the foundation for subsequent selection and stabilization.

Allometry, evolution and development of neocortex size in mammals.

Variation in neocortex size is one of the defining features of mammalian brain evolution. The paramount assumption has been that neocortex size indicates a monotonic allometric relationship with brain size. This assumption holds the concomitant neurodevelopmental assumption that the ontogenetic trajectory of neocortex size is so stable across species that it restrains changes in the direction of evolution. Here we test this fundamental assumption. Whereas previous research has focused exclusively on changes in mean size among groups (i.e., intercept), we additionally investigate changes in covariation (i.e., slope) and strength of allometric integration (i.e., residual variation). We further increase data resolution by investigating 350 species representing 11 mammalian orders. Results identify nine shifts in covariation between neocortex and brainstem in different mammalian groups, indicate that these shifts occur independently of shifts in size, and demonstrate that the strength of allometric integration across different neocortical regions in primates is inversely related to the neurodevelopmental gradient such that later developing regions underwent more evolutionary change. Although our results confirm that variation in brain organization is structured along a neurodevelopmental gradient, our results suggest two additional principles of size reorganization in brain evolution: (1) repatterning of growth allocation among brain regions may occur independently of size and (2) later developing regions indicate faster evolution, not necessarily directional evolution toward larger size. We conclude that the evolution of neocortex size in mammals is far more variable than previously assumed, in turn suggesting a higher degree of evolutionary flexibility in neurodevelopmental patterning than commonly suggested.

Significant Neuroanatomical Variation Among Domestic Dog Breeds.

Humans have bred different lineages of domestic dogs for different tasks such as hunting, herding, guarding, or companionship. These behavioral differences must be the result of underlying neural differences, but surprisingly, this topic has gone largely unexplored. The current study examined whether and how selective breeding by humans has altered the gross organization of the brain in dogs. We assessed regional volumetric variation in MRI studies of 62 male and female dogs of 33 breeds. Neuroanatomical variation is plainly visible across breeds. This variation is distributed nonrandomly across the brain. A whole-brain, data-driven independent components analysis established that specific regional subnetworks covary significantly with each other. Variation in these networks is not simply the result of variation in total brain size, total body size, or skull shape. Furthermore, the anatomy of these networks correlates significantly with different behavioral specialization(s) such as sight hunting, scent hunting, guarding, and companionship. Importantly, a phylogenetic analysis revealed that most change has occurred in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. Together, these results establish that brain anatomy varies significantly in dogs, likely due to human-applied selection for behavior.SIGNIFICANCE STATEMENT Dog breeds are known to vary in cognition, temperament, and behavior, but the neural origins of this variation are unknown. In an MRI-based analysis, we found that brain anatomy covaries significantly with behavioral specializations such as sight hunting, scent hunting, guarding, and companionship. Neuroanatomical variation is not simply driven by brain size, body size, or skull shape, and is focused in specific networks of regions. Nearly all of the identified variation occurs in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. These results indicate that through selective breeding, humans have significantly altered the brains of different lineages of domestic dogs in different ways.

Evolutionary divergence of neuroanatomical organization and related genes in chimpanzees and bonobos.

Given their close genetic relatedness to humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) offer an essential comparative framework for studying the evolution of uniquely human traits. These two species differ markedly in their socio-behavioral repertoires, which is reflected in neuroanatomical differences that have been reported in the literature. However, phylogenetic comparative methods have not yet been used to map the evolution of neuroanatomical traits in bonobos and chimpanzees, limiting our ability to understand which neural systems are derived in each species in relation to the last common ancestor of Pan (Pan-LCA). Here, we examine evolutionary changes in neuroanatomical traits of bonobos and chimpanzees relative to ancestral character reconstructions of the Pan-LCA using comparative datasets from hominoids. We found that bonobo brains are derived in showing reduction of whole brain and white matter volumes, with particularly striking reduction of male brain size compared to the inferred Pan-LCA value. Brain structures related to social cognition and emotional regulation, like the insular cortex and amygdala, display a mosaic pattern of evolution with certain traits changing to a greater extent in each species. Examination of potential genetic mechanisms underlying divergence of neural and social traits did not reveal clear differences in protein evolution patterns between the two species. These findings suggest that the brain anatomy of extant bonobos and chimpanzees show lineage-specific specializations and neither can be considered to more closely retain the ancestral state of Pan. Consequently, this raises questions about the extent that modern chimpanzees or bonobos may serve as referential models for the neuroanatomy of the LCA of humans and apes.

Distinct Patterns of Hippocampal and Neocortical Evolution in Primates.

Because of the central role of the hippocampus in representing spatial and temporal details of experience, comparative studies of its volume and structure are relevant to understanding the evolution of representational memory across species. The hippocampal formation, however, is organized into separate anatomical subregions with distinct functions, and little is known about the evolutionary diversification of these subregions. We investigate relative volumetric changes in hippocampal subregions across a large sample of primate species. We then compare the evolution of the hippocampal formation to the neocortex. Results across hippocampal subregions indicate that, compared to strepsirrhines, the anthropoid lineage displays a decrease in relative CA3, fascia dentata, subiculum, and rhinal cortex volume in tandem with an increase in relative neocortical volume. These findings indicate that hippocampal function in anthropoids might be substantially augmented by the executive decision-making functions of the neocortex. Humans are found to have a unique cerebral organization combining increased relative CA3, subiculum, and rhinal cortex with increased relative neocortical volumes, suggesting that these regions may play a role in behaviors that are uniquely specialized in humans.

Brain size expansion in primates and humans is explained by a selective modular expansion of the cortico-cerebellar system.

Comparative variation in brain size is arguably one of the most dominant features of primate evolution. Enduring questions in this context comprise whether evolutionary changes in certain brain regions outpace changes in other regions, and to what extent such regional variation between species explains comparative variation in overall brain size. To answer this question, we investigate the tempo and mode of evolution of brain organization using the largest combination of brain regions and species analyzed to date (36 brain regions, together representing over 90% of overall brain size, across 17 anthropoid primates, including humans). Following studies suggesting that the expansion of the major constituent regions of the cortico-cerebellar system (CCS) predominantly explain human brain size expansion, we test whether the link between variation in the CCS and brain size is consistent across primates. Results indicate that the constituent brain regions of the CCS show the highest rates of evolution, demonstrate a significant modular pattern of evolution, and closely align with changes in overall brain size. This phenotypic structure is consistent across different taxonomic scales, suggesting that the evolution of anthropoid brain organization is underpinned by a stable genetic structure and is characterized by a conserved evolutionary trajectory towards the CCS. Results hereby suggest that the expansion of the CCS is the primary driver of brain expansion in anthropoid primates. These findings have fundamental implications for our understanding of the nature of primate and human cognition, and the genetic and developmental structure that underpins brain evolution.

Evolutionary pathways toward gigantism in sharks and rays.

Through elasmobranch (sharks and rays) evolutionary history, gigantism evolved multiple times in phylogenetically distant species, some of which are now extinct. Interestingly, the world's largest elasmobranchs display two specializations found never to overlap: filter feeding and mesothermy. The contrasting lifestyles of elasmobranch giants provide an ideal case study to elucidate the evolutionary pathways leading to gigantism in the oceans. Here, we applied a phylogenetic approach to a global dataset of 459 taxa to study the evolution of elasmobranch gigantism. We found that filter feeders and mesotherms deviate from general relationships between trophic level and body size, and exhibit significantly larger sizes than ectothermic-macropredators. We confirm that filter feeding arose multiple times during the Paleogene, and suggest the possibility of a single origin of mesothermy in the Cretaceous. Together, our results elucidate two main evolutionary pathways that enable gigantism: mesothermic and filter feeding. These pathways were followed by ancestrally large clades and facilitated extreme sizes through specializations for enhancing prey intake. Although a negligible percentage of ectothermic-macropredators reach gigantic sizes, these species lack such specializations and are correspondingly constrained to the lower limits of gigantism. Importantly, the very adaptive strategies that enabled the evolution of the largest sharks can also confer high extinction susceptibility.

Neural Correlates of Vocal Repertoire in Primates.

Understanding the nature of the relationship between vocal complexity and brain architecture across non-human primates may help elucidate some of the key elements underlying the evolution of human speech. Here, we report a positive correlation between vocal repertoire size and the relative size of cortical association areas (governing voluntary control over behavioural output) in non-human primates. We further demonstrate that a hominid grade shift in the relative volume of cortical association areas coincides with a similar grade shift in the hypoglossal nucleus (which is associated with the cranial nerve that innervates the muscles of the tongue). Our results support a qualitative continuity in the neural correlates of vocal repertoire, but a quantitative discontinuity in the extent to which the neural system supporting speech is innervated by cortical association areas in great apes and humans.

A cerebellar substrate for cognition evolved multiple times independently in mammals.

Given that complex behavior evolved multiple times independently in different lineages, a crucial question is whether these independent evolutionary events coincided with modifications to common neural systems. To test this question in mammals, we investigate the lateral cerebellum, a neurobiological system that is novel to mammals, and is associated with higher cognitive functions. We map the evolutionary diversification of the mammalian cerebellum and find that relative volumetric changes of the lateral cerebellar hemispheres (independent of cerebellar size) are correlated with measures of domain-general cognition in primates, and are characterized by a combination of parallel and convergent shifts towards similar levels of expansion in distantly related mammalian lineages. Results suggest that multiple independent evolutionary occurrences of increased behavioral complexity in mammals may at least partly be explained by selection on a common neural system, the cerebellum, which may have been subject to multiple independent neurodevelopmental remodeling events during mammalian evolution.

The coevolution of play and the cortico-cerebellar system in primates.

Primates are some of the most playful animals in the natural world, yet the reason for this remains unclear. One hypothesis posits that primates are so playful because playful activity functions to help develop the sophisticated cognitive and behavioural abilities that they are also renowned for. If this hypothesis were true, then play might be expected to have coevolved with the neural substrates underlying these abilities in primates. Here, we tested this prediction by conducting phylogenetic comparative analyses to determine whether play has coevolved with the cortico-cerebellar system, a neural system known to be involved in complex cognition and the production of complex behaviour. We used phylogenetic generalised least squares analyses to compare the relative volume of the largest constituent parts of the primate cortico-cerebellar system (prefrontal cortex, non-prefrontal heteromodal cortical association areas, and posterior cerebellar hemispheres) to the mean percentage of time budget spent in play by a sample of primate species. Using a second categorical data set on play, we also used phylogenetic analysis of covariance to test for significant differences in the volume of the components of the cortico-cerebellar system among primate species exhibiting one of three different levels of adult-adult social play. Our results suggest that, in general, a positive association exists between the amount of play exhibited and the relative size of the main components of the cortico-cerebellar system in our sample of primate species. Although the explanatory power of this study is limited by the correlational nature of its analyses and by the quantity and quality of the data currently available, this finding nevertheless lends support to the hypothesis that play functions to aid the development of cognitive and behavioural abilities in primates.