Course Of Primate Evolution Research Articles

Might pain be experienced in the brainstem rather than in the cerebral cortex?

It is nearly axiomatic that pain, among other examples of conscious experience, is an outcome of still-uncertain forms of neural processing that occur in the cerebral cortex, and specifically within thalamo-cortical networks. This belief rests largely on the dramatic relative expansion of the cortex in the course of primate evolution, in humans in particular, and on the fact that direct activation of sensory representations in the cortex evokes a corresponding conscious percept. Here we assemble evidence, drawn from a number of sources, suggesting that pain experience is unlike the other senses and may not, in fact, be an expression of cortical processing. These include the virtual inability to evoke pain by cortical stimulation, the rarity of painful auras in epileptic patients and outcomes of cortical lesions. And yet, pain perception is clearly a function of a conscious brain. Indeed, it is perhaps the most archetypical example of conscious experience. This draws us to conclude that conscious experience, at least as realized in the pain system, is seated subcortically, perhaps even in the “primitive” brainstem. Our conjecture is that the massive expansion of the cortex over the course of evolution was not driven by the adaptive value of implementing consciousness. Rather, the cortex evolved because of the adaptive value of providing an already existing subcortical generator of consciousness with a feed of critical information that requires the computationally intensive capability of the cerebral cortex.

Heteropaternity of twins in ring-tailed lemurs (Lemur catta).

This project investigated paternity among 14 sets of twins born into a colony of ring-tailed lemurs (Lemur catta) on St. Catherines Island, GA. Female L. catta commonly mate with >1 male, and twins of different sexes confirm that dizygotic twinning can occur in this species. However, no study has previously evaluated twins using genetic data to measure the proportion of mono versus dizygotic twinning in L. catta, and no study has tested for heteropaternity (sirehood by two different males) in this species. We predicted that L. catta would show a predominance of dizygosity and evidence for heteropaternity. Paternity was determined for 28 infants (14 sets of twins) via paternity exclusion analyses using 10 polymorphic microsatellite markers, and data were collected on sexual behavior across four mating seasons during the first cycle of mating in each year, which overlapped with the conceptive periods of these infants. All twins were found to be dizygotic, as evidenced by dissimilar multilocus genotypes between the two infants of each twin pair. Heteropaternity was found in 3 of 14 (21% of) twin pairs, whereas the remaining 11 pairs of twins (79%) shared the same sire. In one case of heteropaternity, one sire was a resident male, and one sire was an extra-group male. An extra-group male also sired one of the same-sire twin pairs. All other sires of twins were group residents. Female multiple mating, which is common to many primates including L. catta, can be viewed as an adaptive reproductive strategy whose function-in addition to fertility assurance or stimulating sperm competition-may be to increase the genetic diversity of a female's offspring, even among infants born in the same birth event. Therefore, during the course of primate evolution, the adaptive benefits of heteropaternity would be expected to have contributed to positive selection for female promiscuity.

Postcopulatory sexual selection influences baculum evolution in primates and carnivores.

The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection (particularly, high levels of postcopulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum length evolution within the primate order. We then test the effects of testes mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ancestral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intromission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer bacula in primates. These results suggest the baculum plays an important role in facilitating reproductive strategies in populations with high levels of postcopulatory sexual selection.

Human Cerebellar Sub-millimeter Diffusion Imaging Reveals the Motor and Non-motor Topography of the Dentate Nucleus.

The reciprocal cortico-cerebellar loops that underlie cerebellar contributions to motor and cognitive behavior form one of the largest systems in the primate brain. Work with non-human primates has shown that the dentate nucleus, the major output nucleus of the cerebellum, contains topographically distinct connections to both motor and non-motor regions, yet there is no evidence for how the cerebellar cortex connects to the dentate nuclei in humans. Here we used in-vivo sub-millimeter diffusion imaging to characterize this fundamental component of the cortico-cerebellar loop, and identified a pattern of superior motor and infero-lateral non-motor connectivity strikingly similar to that proposed by animal work. Crucially, we also present first evidence that the dominance for motor connectivity observed in non-human primates may be significantly reduced in man - a finding that is in accordance with the proposed increase in cerebellar contributions to higher cognitive behavior over the course of primate evolution.

Mirror Neurons in a New World Monkey, Common Marmoset.

Mirror neurons respond when executing a motor act and when observing others' similar act. So far, mirror neurons have been found only in macaques, humans, and songbirds. To investigate the degree of phylogenetic specialization of mirror neurons during the course of their evolution, we determined whether mirror neurons with similar properties to macaques occur in a New World monkey, the common marmoset (Callithrix jacchus). The ventral premotor cortex (PMv), where mirror neurons have been reported in macaques, is difficult to identify in marmosets, since no sulcal landmarks exist in the frontal cortex. We addressed this problem using “in vivo” connection imaging methods. That is, we first identified cells responsive to others' grasping action in a clear landmark, the superior temporal sulcus (STS), under anesthesia, and injected fluorescent tracers into the region. By fluorescence stereomicroscopy, we identified clusters of labeled cells in the ventrolateral frontal cortex, which were confirmed to be within the ventrolateral frontal cortex including PMv after sacrifice. We next implanted electrodes into the ventrolateral frontal cortex and STS and recorded single/multi-units under an awake condition. As a result, we found neurons in the ventrolateral frontal cortex with characteristic “mirror” properties quite similar to those in macaques. This finding suggests that mirror neurons occur in a common ancestor of New and Old World monkeys and its common properties are preserved during the course of primate evolution.

Evidence for a vestigial pinna-orienting system in humans.

Although some people can voluntarily move their ears, overt reflexive control of the pinnae has been lost during the course of primate evolution. Humans and apes do not move their ears to express emotion, they do not defensively retract them when startled, and they do not point them at novel, salient, or task-relevant stimuli. Nevertheless, it is the thesis of this review that neural circuits for pinna orienting have survived in a purely vestigial state for over 25 million years. There are three lines of evidence: (1) Shifting the eyes hard to one side is accompanied by electromyographic (EMG) activity in certain ear muscles and by a barely visible (2-3 mm) curling of the dorsal edge of the pinna. (2) The capture of attention by a novel, unexpected sound emanating from behind and to one side has been found to trigger a weak EMG response in the muscle behind the corresponding ear. (3) Reflexive EMG bursts recorded during a selective attention task suggested that subjects were unconsciously attempting to orient their ears toward the relevant sounds. In addition to pinna orienting, the possibility that pinna startle might have survived in a vestigial state is also considered. It is suggested that the postauricular reflex to sudden, intense sounds constitutes a vestigial startle response, but that the reflex arc is dominated by a pathway that bypasses the main organizing center for startle.

Estrogen regulation of microcephaly genes and evolution of brain sexual dimorphism in primates.

BackgroundSexual dimorphism in brain size is common among primates, including humans, apes and some Old World monkeys. In these species, the brain size of males is generally larger than that of females. Curiously, this dimorphism has persisted over the course of primate evolution and human origin, but there is no explanation for the underlying genetic controls that have maintained this disparity in brain size.ResultsIn the present study, we tested the effect of the female hormone (estradiol) on seven genes known to be related to brain size in both humans and nonhuman primates, and we identified half estrogen responsive elements (half EREs) in the promoter regions of four genes (MCPH1, ASPM, CDK5RAP2 and WDR62). Likewise, at sequence level, it appears that these half EREs are generally conserved across primates. Later testing via a reporter gene assay and cell-based endogenous expression measurement revealed that estradiol could significantly suppress the expression of the four affected genes involved in brain size. More intriguingly, when the half EREs were deleted from the promoters, the suppression effect disappeared, suggesting that the half EREs mediate the regulation of estradiol on the brain size genes. We next replicated these experiments using promoter sequences from chimpanzees and rhesus macaques, and observed a similar suppressive effect of estradiol on gene expression, suggesting that this mechanism is conserved among primate species that exhibit brain size dimorphism.ConclusionsBrain size dimorphism among certain primates, including humans, is likely regulated by estrogen through its sex-dependent suppression of brain size genes during development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0398-x) contains supplementary material, which is available to authorized users.

Current research on the organization and function of the visual system in primates.

Current research on the organization and function of the visual system in primates Jon H Kaas, Pooja Balaram Department of Psychology, Vanderbilt University, Nashville, TN, USAAll primates, including humans, are highly visual creatures.1–3 We rely heavily on visual cues for basic adaptive behaviors such as finding food, mates, and shelter; as well as more complex behaviors such as parental care and the formation of social hierarchies. Throughout the course of primate evolution, our dependence on visual cues has increased with each adaptive advantage acquired from visually guided behavior; and so has the demand for greater and more efficient processing of visual information in primate brains. Consequently, the number, size, and complexity of brain structures involved in visual processing has expanded dramatically in the primate order, far more than those of any other species in the mammalian lineage.2,4 As we have learned to interact with the world using visual cues, our brains have evolved to absorb, manipulate, and react to visual information in increasingly effective ways. Individual brain structures dedicated to vision in primates also frequently exhibit anatomical and functional specializations that are not present in other mammals. These adaptations are not present in most nonprimate mammals, partly because many species rely on other sensory modalities for their individual behaviors. Thus, understanding how we, as humans, perceive the visual world around us begins with learning how vision is processed in the primate brain. Furthermore, learning how vision in primates differs both structurally and functionally from vision in nonprimate mammals, and determining how those changes enable adaptive traits in the primate lineage, will allow us to understand the truly unique phenomenon of human visual behavior.

Proteogenomic Review of the Changes in Primate apoC-I during Evolution.

Apolipoprotein C-I has evolved more rapidly than any of the other soluble apolipoproteins. During the course of primate evolution, the gene for this apolipoprotein was duplicated. Prompted by our observation that the two resulting genes encode two distinct forms of apoC-I in great apes, we have reviewed both the genomic and proteomic data to examine what changes have occurred during the course of primate evolution. We have found data showing that one of the duplicated genes, known to be a pseudogene in humans, was also a pseudogene in Denisovans and Neandertals. Using genomic and proteomic data for primates, we will provide in this review evidence that the duplication took place after the divergence of New World monkeys from the human lineage and that the formation of the pseudogene took place after the divergence of the bonobos and chimpanzees from the human lineage.

The function and evolution of the restriction factor viperin in primates was not driven by lentiviruses

BackgroundViperin, also known as RSAD2, is an interferon-inducible protein that potently restricts a broad range of different viruses such as influenza, hepatitis C virus, human cytomegalovirus and West Nile virus. Viperin is thought to affect virus budding by modification of the lipid environment within the cell. Since HIV-1 and other retroviruses depend on lipid domains of the host cell for budding and infectivity, we investigated the possibility that Viperin also restricts human immunodeficiency virus and other retroviruses.ResultsLike other host restriction factors that have a broad antiviral range, we find that viperin has also been evolving under positive selection in primates. The pattern of positive selection is indicative of Viperin's escape from multiple viral antagonists over the course of primate evolution. Furthermore, we find that Viperin is interferon-induced in HIV primary target cells. We show that exogenous expression of Viperin restricts the LAI strain of HIV-1 at the stage of virus release from the cell. Nonetheless, the effect of Viperin restriction is highly strain-specific and does not affect most HIV-1 strains or other retroviruses tested. Moreover, knockdown of endogenous Viperin in a lymphocytic cell line did not significantly affect the spreading infection of HIV-1.ConclusionDespite positive selection having acted on Viperin throughout primate evolution, our findings indicate that Viperin is not a major restriction factor against HIV-1 and other retroviruses. Therefore, other viral lineages are likely responsible for the evolutionary signatures of positive selection in viperin among primates.

Active Vision: Fixational Eye Movements Help Seeing Space in Time

The significance of the miniature eye movements that we make during visual fixation has been intensely debated for the last 80 years. Recent studies have revealed that these motions of the eyes fulfill an important functional role: helping to extract useful information from natural scenes.

Paw preference is not affected by postural demand in a nonprimate mammal (Felis silvestris catus).

Previously, it has been thought that handedness is unique to humans. Recently, it has been found that hand or paw preferences are common among a variety of vertebrate species. Different models have been put forth to describe the evolution of primate handedness. In this study we aimed to explore whether these models can also be used to predict manual laterality in nonprimate mammalian groups. The cat (Felis silvestris catus) is a good nonprimate model for manual laterality, as cats frequently use paws to catch and hold prey. Cats were exposed to two standardized manual laterality tasks, differing in postural demand. Subjects (N = 28) were forced to use either a stable or unstable body posture (i.e., sitting or standing vs. vertical clinging) to extract food items from a plastic box attached at two different heights. We revealed that cats exhibited paw preferences at an individual level with about 40% left, 30% right, 30% nonlateralized subjects. Postural demand was linked to task difficulty: the unstable body posture was found to be significantly more difficult than the stable body posture. However, these differences in postural demand and task difficulty did not lead to differences in direction or strength of paw preference. Findings suggested that nonprimate mammals differ from primates in their sensitivity to task related factors, such as postural demand. Results coincide with those of some prosimians, providing support for the hypothesis that postural demand and the associated task complexity became influencing factors on manual laterality in the course of primate evolution.

Signatures of Natural Selection in a Primate Bitter Taste Receptor

Bitter taste receptors (TAS2Rs) enable animals to detect and avoid toxins in the environment, including noxious defense compounds produced by plants. This suggests that TAS2Rs are under complex pressures from natural selection. To investigate these pressures, we examined signatures of selection in the primate TAS2R38 gene. Whole-gene (1,002 bp) sequences from 40 species representing all major primate taxa uncovered extensive variation. Nucleotide substitutions occurred at 448 positions, resulting in 201 amino acid changes. Two single-nucleotide deletions, one three-nucleotide in-frame deletion, and one premature stop codon were also observed. The rate of non-synonymous substitution (ω = dN/dS), was high in TAS2R38 (ω = 0.60) compared to other genes, but significantly lower than expected under neutrality (P = 4.0 × 10(-9)), indicating that purifying selection has maintained the basic structure of the receptor. However, differences were present among receptor subregions. Non-synonymous rates were significantly lower than expected in transmembrane domains (ω = 0.55, P = 1.18 × 10(-12)) and internal loops (ω = 0.51, P = 7.04 × 10(-5)), but not external loops (ω = 1.16, P = 0.53), and evidence of positive selection was found in external loop 2, which exhibited a high rate (ω = 2.53) consistent with rapid shifts in ligand targeting. These patterns point to a history of rapid yet constrained change in bitter taste responses in the course of primate evolution.

Molecular evolution of immunoglobulin superfamily genes in primates

Genes of the immunoglobulin superfamily (IgSF) have a wide variety of cellular activities. In this study, we investigated molecular evolution of IgSF genes in primates by comparing orthologous sequences of 249 IgSF genes among human, chimpanzee, orangutan, rhesus macaque, and common marmoset. To evaluate the non-synonymous/synonymous substitution ratio (ω), we applied Bn-Bs program and PAML program. IgSF genes were classified into 11 functional categories based on the Gene Ontology (GO) database. Among them, IgSF genes in three functional categories, immune system process (GO:0002376), defense response (GO:0006952), and multi-organism process (GO:0051704), which are tightly linked to the regulation of immune system had much higher values of ω than genes in the other GO categories. In addition, we estimated the average values of ω for each primate lineage. Although each primate lineage had comparable average values of ω, the human lineage showed the lowest ω value for the immune-related genes. Furthermore, 11 IgSF genes, SIGLEC5, SLAMF6, CD33, CD3E, CEACAM8, CD3G, FCER1A, CD48, CD4, TIM4, and FCGR2A, were implied to have been under positive selective pressure during the course of primate evolution. Further sequence analyses of CD3E and CD3G from 23 primate species suggested that the Ig domains of CD3E and CD3G underwent the positive Darwinian selection.

Cochlear Labyrinth Volume in Euarchontoglirans: Implications for the Evolution of Hearing in Primates

Using high resolution X-ray computed tomography data we examined the relationship between cochlear labyrinth volume and body mass in extant, non-primate euarchontoglirans, and in two fossils, to allow for comparison with the results of Kirk and Gosselin-Ildari (2009). Modern primates have significantly higher cochlear labyrinth volumes relative to body mass than other euarchontoglirans, which may be related to a downward shift in the highest and lowest audible frequencies over the course of primate evolution, and to the relative increase in brain size observed in Euprimates.

Consistent levels of A-to-I RNA editing across individuals in coding sequences and non-conserved Alu repeats

BackgroundAdenosine to inosine (A-to-I) RNA-editing is an essential post-transcriptional mechanism that occurs in numerous sites in the human transcriptome, mainly within Alu repeats. It has been shown to have consistent levels of editing across individuals in a few targets in the human brain and altered in several human pathologies. However, the variability across human individuals of editing levels in other tissues has not been studied so far.ResultsHere, we analyzed 32 skin samples, looking at A-to-I editing level in three genes within coding sequences and in the Alu repeats of six different genes. We observed highly consistent editing levels across different individuals as well as across tissues, not only in coding targets but, surprisingly, also in the non evolutionary conserved Alu repeats.ConclusionsOur findings suggest that A-to-I RNA-editing of Alu elements is a tightly regulated process and, as such, might have been recruited in the course of primate evolution for post-transcriptional regulatory mechanisms.

Basic mathematical rules are encoded by primate prefrontal cortex neurons

Mathematics is based on highly abstract principles, or rules, of how to structure, process, and evaluate numerical information. If and how mathematical rules can be represented by single neurons, however, has remained elusive. We therefore recorded the activity of individual prefrontal cortex (PFC) neurons in rhesus monkeys required to switch flexibly between "greater than" and "less than" rules. The monkeys performed this task with different numerical quantities and generalized to set sizes that had not been presented previously, indicating that they had learned an abstract mathematical principle. The most prevalent activity recorded from randomly selected PFC neurons reflected the mathematical rules; purely sensory- and memory-related activity was almost absent. These data show that single PFC neurons have the capacity to represent flexible operations on most abstract numerical quantities. Our findings support PFC network models implementing specific "rule-coding" units that control the flow of information between segregated input, memory, and output layers. We speculate that these neuronal circuits in the monkey lateral PFC could readily have been adopted in the course of primate evolution for syntactic processing of numbers in formalized mathematical systems.

Inhibitory interneurons of the human prefrontal cortex display conserved evolution of the phenotype and related genes

Inhibitory interneurons participate in local processing circuits, playing a central role in executive cognitive functions of the prefrontal cortex. Although humans differ from other primates in a number of cognitive domains, it is not currently known whether the interneuron system has changed in the course of primate evolution leading to our species. In this study, we examined the distribution of different interneuron subtypes in the prefrontal cortex of anthropoid primates as revealed by immunohistochemistry against the calcium-binding proteins calbindin, calretinin and parvalbumin. In addition, we tested whether genes involved in the specification, differentiation and migration of interneurons show evidence of positive selection in the evolution of humans. Our findings demonstrate that cellular distributions of interneuron subtypes in human prefrontal cortex are similar to other anthropoid primates and can be explained by general scaling rules. Furthermore, genes underlying interneuron development are highly conserved at the amino acid level in primate evolution. Taken together, these results suggest that the prefrontal cortex in humans retains a similar inhibitory circuitry to that in closely related primates, even though it performs functional operations that are unique to our species. Thus, it is likely that other significant modifications to the connectivity and molecular biology of the prefrontal cortex were overlaid on this conserved interneuron architecture in the course of human evolution.

Organization of the posterior parietal cortex in galagos: I. Functional zones identified by microstimulation

We used half-second trains of intracortical microstimulation to study the functional organization of the posterior parietal cortex (PPC) in prosimian galagos. These trains of current pulses evoked meaningful behaviors from the anterior, but not posterior, half of PPC. Stimulation of dorsal PPC caused contralateral forelimb movements, including defensive, hand-to-mouth, and reaching movements. Defensive and hand-to-mouth movement territories overlapped, although hand-to-mouth movements were usually evoked from more rostrolateral sites than defensive movements. Reaching movement sites were typically more caudal than defensive or hand-to-mouth movement sites. Stimulation of the most medial PPC sites evoked complex movements of forelimbs and hindlimbs. Ventral PPC commonly represented defensive face movements. Similar defensive movements, with the addition of widely opening the mouth to expose the teeth, were elicited from a small area in front of the PPC defensive face zone. Sometimes defensive face movements occurred with forelimb movements. Thus, subregions of PPC relate to different ethologically relevant categories of behavior. Most movements were initiated within 33-100 msec after stimulus onset. Face, eye blink, and ear movements were generally less delayed than forelimb movements. The present results in galagos, together with those obtained from macaque monkeys by Graziano and coworkers (Graziano et al. [2002a] Neuron 34:841-851; Cooke et al., [2003] Proc. Natl. Acad. Sci. U.S.A. 100:6163-6168), suggest that the functional involvement of the PPC in specific types of sensorimotor behavior evolved early in the course of primate evolution and that networks for complex movements involving motor and posterior parietal areas are characteristic of all primate brains.

Differences in DNA Methylation Patterns and Expression of the CCRK Gene in Human and Nonhuman Primate Cortices

Changes in DNA methylation patterns during embryo development and differentiation processes are linked to the transcriptional plasticity of our genome. However, little is known about the evolutionary conservation of DNA methylation patterns and the evolutionary impact of epigenetic differences between closely related species. Here we compared the methylation patterns of CpG islands (CGIs) in the promoter regions of seven genes in humans and chimpanzees. We identified a block of CpGs in the cell cycle-related kinase (CCRK) gene that is more methylated in the adult human cortex than in the chimpanzee cortex and, in addition, it exhibits considerable intraspecific variation both in humans and chimpanzees. The species-specifically methylated region (SMR) lies between the almost completely methylated 5' region and the completely demethylated 3' region of the presumed CCRK CGI promoter. It is part of an Alu-Sg1 repeat that has been integrated into the promoter region in a common ancestor of humans and New World monkeys. This SMR is relatively hypomethylated in the rhesus monkey cortex and more or less completely methylated in the baboon cortex, indicating extraordinary methylation dynamics during primate evolution. The mRNA expression level of CCRK has also changed during the course of primate evolution. CCRK is expressed at much higher levels in human and baboon cortices, which display an average SMR methylation of 70% and 100%, respectively, than in chimpanzee and rhesus macaque cortices with an average SMR methylation of 35% and 40%, respectively. The observed evolutionary dynamics suggests a possibility that CCRK has been important for evolution of the primate brain.