Mental evolution and development: Evidence for secondary representation in children, great apes, and other animals

Recent interest in the development and evolution of theory of mind has provided a wealth of information about representational skills in both children and animals, According to J, Perrier (1991), children begin to entertain secondary representations in the 2nd year of life. This advance manifests in their passing hidden displacement tasks, engaging in pretense and means-ends reasoning, interpreting external representations, displaying mirror self-recognition and empathic behavior, and showing an early understanding of mind and imitation. New data show a cluster of mental accomplishments in great apes that is very similar to that observed in 2-year-old humans. It is suggested that it is most parsimonious to assume that this cognitive profile is of homologous origin and that great apes possess secondary representational capacity. Evidence from animals other than apes is scant. This analysis leads to a number of predictions for future research.

Rapid evolution of the cerebellum in humans and other great apes

Humans’ unique cognitive abilities are usually attributed to a greatly expanded neocortex, which has been described as “the crowning achievement of evolution and the biological substrate of human mental prowess” [1]. The human cerebellum, however, contains four times more neurons than the neocortex [2] and is attracting increasing attention for its wide range of cognitive functions. Using a method for detecting evolutionary rate changes along the branches of phylogenetic trees, we show that the cerebellum underwent rapid size increase throughout the evolution of apes, including humans, expanding significantly faster than predicted by the change in neocortex size. As a result, humans and other apes deviated significantly from the general evolutionary trend for neocortex and cerebellum to change in tandem, having significantly larger cerebella relative to neocortex size than other anthropoid primates. These results suggest that cerebellar specialization was a far more important component of human brain evolution than hitherto recognized and that technical intelligence was likely to have been at least as important as social intelligence in human cognitive evolution. Given the role of the cerebellum in sensory-motor control and in learning complex action sequences, cerebellar specialization is likely to have underpinned the evolution of humans’ advanced technological capacities, which in turn may have been a preadaptation for language.

Properties of tooth enamel in great apes

A comparative study has been made of human and great ape molar tooth enamel. Nanoindentation techniques are used to map profiles of elastic modulus and hardness across sections from the enamel–dentin junction to the outer tooth surface. The measured data profiles overlap between species, suggesting a degree of commonality in material properties. Using established deformation and fracture relations, critical loads to produce function-threatening damage in the enamel of each species are calculated for characteristic tooth sizes and enamel thicknesses. The results suggest that differences in load-bearing capacity of molar teeth in primates are less a function of underlying material properties than of morphology.

Fluorescence in situ hybridization analysis of keratinocyte growth factor gene amplification and dispersion in evolution of great apes and humans

Keratinocyte growth factor (KGF) is a member of the fibroblast growth factor family. Portions of the gene encoding KGF were amplified during primate evolution and are present in multiple nonprocessed copies in the human genome. Nucleotide analysis of a representative sampling of these KGF-like sequences indicated that they were at least 95% identical to corresponding regions of the KGF gene. To localize these sequences to specific chromosomal sites in human and higher primates, we used fluorescence in situ hybridization. In human, using a cosmid probe encoding KGF exon 1, we assigned the location of the KGF gene to chromosome 15q15–21.1. In addition, copies of KGF-like sequences hybridizing only with a cosmid probe encoding exons 2 and 3 were localized to dispersed sites on chromosome 2q21, 9p11, 9q12–13, 18p11, 18q11, 21q11, and 21q21.1. The distribution of KGF-like sequences suggests a role for alphoid DNA in their amplification and dispersion. In chimpanzee, KGF-like sequences were observed at five chromosomal sites, which were each homologous to sites in human, while in gorilla, a subset of four of these homologous sites was identified; in orangutan two sites were identified, while gibbon exhibited only a single site. The chromosomal localization of KGF sequences in human and great ape genomes indicates that amplification and dispersion occurred in multiple discrete steps, with initial KGF gene duplication and dispersion taking place in gibbon and involving loci corresponding to human chromosomes 15 and 21. These findings support the concept of a closer evolutionary relationship of human and chimpanzee and a possible selective pressure for such dispersion during the evolution of higher primates.

A burst of segmental duplications in the genome of the African great ape ancestor

It is generally accepted that the extent of phenotypic change between human and great apes is dissonant with the rate of molecular change. Between these two groups, proteins are virtually identical, cytogenetically there are few rearrangements that distinguish ape-human chromosomes, and rates of single-base-pair change and retrotransposon activity have slowed particularly within hominid lineages when compared to rodents or monkeys. Studies of gene family evolution indicate that gene loss and gain are enriched within the primate lineage. Here, we perform a systematic analysis of duplication content of four primate genomes (macaque, orang-utan, chimpanzee and human) in an effort to understand the pattern and rates of genomic duplication during hominid evolution. We find that the ancestral branch leading to human and African great apes shows the most significant increase in duplication activity both in terms of base pairs and in terms of events. This duplication acceleration within the ancestral species is significant when compared to lineage-specific rate estimates even after accounting for copy-number polymorphism and homoplasy. We discover striking examples of recurrent and independent gene-containing duplications within the gorilla and chimpanzee that are absent in the human lineage. Our results suggest that the evolutionary properties of copy-number mutation differ significantly from other forms of genetic mutation and, in contrast to the hominid slowdown of single-base-pair mutations, there has been a genomic burst of duplication activity at this period during human evolution.

The Influence of Fallback Foods on Great Ape Tooth Enamel

Lucas and colleagues recently proposed a model based on fracture and deformation concepts to describe how mammalian tooth enamel may be adapted to the mechanical demands of diet (Lucas et al.: Bioessays 30[2008] 374-385). Here we review the applicability of that model by examining existing data on the food mechanical properties and enamel morphology of great apes (Pan, Pongo, and Gorilla). Particular attention is paid to whether the consumption of fallback foods is likely to play a key role in influencing great ape enamel morphology. Our results suggest that this is indeed the case. We also consider the implications of this conclusion on the evolution of the dentition of extinct hominins.

Apes’ tracking of objects and collections

Recent research suggests that great apes are less vulnerable to cohesion violations than human infants are. In contrast to human infants, apes successfully track nonsolid substances or split solid objects through occlusion (Cacchione & Call, 2010a; Cacchione, Hrubesch, & Call, 2012, 2013). The present study aims to investigate whether the lower vulnerability of great apes to cohesion violations also manifests when they are tracking collections. While even very young human infants appreciate the continuous existence of solid bound objects, they fail to show similar intuitions when tracking collections of objects (Chiang & Wynn, 2000). In a manual search task inspired by recent infant research, we tested whether humans’ closest relatives, the great apes, showed a similar contrast in their reasoning about single solid objects and objects within collections. The results suggest that, in contrast to human infants, great apes appreciate the continuous existence of objects within collections and successfully track them through occlusion. This confirms the view that great apes are generally less vulnerable to cohesion violations than human infants.

Immunodetection of Helicobacter sp. and the associated expression of ABO blood group antigens in the gastric mucosa of captive and free-living New World primates in the Amazon region

The histo-blood group ABH antigens were first described in humans. These antigens are only present on erythrocytes from great apes and humans, while in more primitive animals they are found in tissues and body fluids. The ABH antigens are mainly distributed in tissues exposed to the external environment and potentially serve as ligands for pathogens or inhibitors of tissue connections. The objective of this paper was two-fold: (i) to determine the presence of Helicobacter sp. in the gastric mucosa of 16 captive and 24 free-living New World monkeys and (ii) to evaluate the presence of histopathological alterations related to bacterial infection and the associated expression of ABH antigens in the tissue. Stomach tissues from 13 species of monkey were assessed using haematoxylin-eosin and modified Gram staining (Hucker) methods. An immunohistochemical analysis of the tissue revealed the presence of infectious bacteria that were characteristic of the genus Helicobacter sp. The results demonstrate that various species of monkey might be naturally infected with the Helicobacter sp. and that there is an increased susceptibility to infection. This study serves as a comparative analysis of infection between human and non-human primates and indicates the presence of a new species of Helicobacter.

Evolutionary and Functional Analyses of the Interaction between the Myeloid Restriction Factor SAMHD1 and the Lentiviral Vpx Protein.

SAMHD1 has recently been identified as an HIV-1 restriction factor operating in myeloid cells. As a countermeasure, the Vpx accessory protein from HIV-2 and certain lineages of SIV have evolved to antagonize SAMHD1 by inducing its ubiquitin-proteasome-dependent degradation. Here, we show that SAMHD1 experienced strong positive selection episodes during primate evolution that occurred in the Catarrhini ancestral branch prior to the separation between hominoids (gibbons and great apes) and Old World monkeys. The identification of SAMHD1 residues under positive selection led to mapping the Vpx-interaction domain of SAMHD1 to its C-terminal region. Importantly, we found that while SAMHD1 restriction activity toward HIV-1 is evolutionarily maintained, antagonism of SAMHD1 by Vpx is species-specific. The distinct evolutionary signature of SAMHD1 sheds light on the development of its antiviral specificity.

Neogene antecedents of the modern human hand and its relation to bipedalism

El present projecte s'ha dut a terme a l'American Museum of Natural History (AMNH, New York) entre el 31 de Desembre de 2010 i el 30 de Desembre de 2012. L'objectiu del projecte era elucidar la història evolutiva de la mà humana: traçar els canvis evolutius en la seva forma i proporcions que van propiciar la seva estructura moderna que permet als humans manipular amb precisió. El treball realitzat ha inclòs recol•lecció de dades i anàlisis, redacció de resultats i formació en mètodes analítics específics. Durant aquest temps, l'autor a completat la seva de base de dades existent en mesures lineals de la mà a hominoides. També s'han agafat dades del peu; d'aquesta forma ara mateix es compta amb una base de dades amb més de 500 individus, amb més de 200 mesures per cada un. També s'han agafat dades en tres imensions utilitzant un làser escàner. S'han après tècniques de morfometria geomètrica 3D directament dels pioners al camp a l'AMNH. Com a resultat d'aquesta feina s'han produït 10 resums (publicats a congressos internacionals) i 9 manuscrits (molts d'ells ja publicats a revistes internacionals) amb resultats de gran rellevància: La mà humana posseeix unes proporcions relativament primitives, que són més similars a les proporciones que tenien els hominoides fòssils del Miocè que no pas a la dels grans antropomorfs actuals. Els darrers tenen unes mans allargades amb un polzes molt curts que reflexen l'ús de la mà com a eina de suspensió sota les branques. En canvi, els hominoides del Miocè tenien unes mans relativament curtes amb un polze llarg que feien servir per estabilitzar el seu pes quan caminaven per sobre de les branques. Una vegada els primers homínids van aparèixer al final del Miocè (fa uns 6 Ma) i van començar a fer servir el bipedisme com a mitjà més comú de locomoció, les seves mans van ser "alliberades" de les seves funcions locomotores. La selecció natural—ara només treballant en la manipulació—va convertir les proporcions ja existents de la mà d'aquests primats en l'òrgan manipulatori que representa la mà humana avui dia.

Characterization and evolution of the novel gene family FAM90A in primates originated by multiple duplication and rearrangement events

Genomic plasticity of human chromosome 8p23.1 region is highly influenced by two groups of complex segmental duplications (SDs), termed REPD and REPP, that mediate different kinds of rearrangements. Part of the difficulty to explain the wide range of phenotypes associated with 8p23.1 rearrangements is that REPP and REPD are not yet well characterized, probably due to their polymorphic status. Here, we describe a novel primate-specific gene family, named FAM90A (family with sequence similarity 90), found within these SDs. According to the current human reference sequence assembly, the FAM90A family includes 24 members along 8p23.1 region plus a single member on chromosome 12p13.31, showing copy number variation (CNV) between individuals. These genes can be classified into subfamilies I and II, which differ in their upstream and 5′-untranslated region sequences, but both share the same open reading frame and are ubiquitously expressed. Sequence analysis and comparative fluorescence in situ hybridization studies showed that FAM90A subfamily II suffered a big expansion in the hominoid lineage, whereas subfamily I members were likely generated sometime around the divergence of orangutan and African great apes by a fusion process. In addition, the analysis of the Ka/Ks ratios provides evidence of functional constraint of some FAM90A genes in all species. The characterization of the FAM90A gene family contributes to a better understanding of the structural polymorphism of the human 8p23.1 region and constitutes a good example of how SDs, CNVs and rearrangements within themselves can promote the formation of new gene sequences with potential functional consequences.

Death and resurrection of the human IRGM gene

Immunity-related GTPases (IRG) play an important role in defense against intracellular pathogens. One member of this gene family in humans, IRGM, has been recently implicated as a risk factor for Crohn's disease. We analyzed the detailed structure of this gene family among primates and showed that most of the IRG gene cluster was deleted early in primate evolution, after the divergence of the anthropoids from prosimians ( about 50 million years ago). Comparative sequence analysis of New World and Old World monkey species shows that the single-copy IRGM gene became pseudogenized as a result of an Alu retrotransposition event in the anthropoid common ancestor that disrupted the open reading frame (ORF). We find that the ORF was reestablished as a part of a polymorphic stop codon in the common ancestor of humans and great apes. Expression analysis suggests that this change occurred in conjunction with the insertion of an endogenous retrovirus, which altered the transcription initiation, splicing, and expression profile of IRGM. These data argue that the gene became pseudogenized and was then resurrected through a series of complex structural events and suggest remarkable functional plasticity where alleles experience diverse evolutionary pressures over time. Such dynamism in structure and evolution may be critical for a gene family locked in an arms race with an ever-changing repertoire of intracellular parasites.

Lipoprotéine(a): de l'athérosclérose à Alzheimer [Lipoprotein (a) in Alzheimer's atherosclerosis].

Lipoprotein(a) [Lp(a)] is an enigmatic lipoprotein particle present in the plasma from humans, great apes and hedgehogs. Plasma levels of Lp(a) vary widely between individuals and are largely determined by specific sequences within the gene encoding apo(a), the unique highly polymorphic glycoprotein attached to apoB of low density lipoprotein (LDL) to form Lp(a). Elevated plasma concentrations of LP(a) are associated with the premature development of atherosclerosis. A major goal of our laboratory is to better understand the metabolism of Lp(a) and its function in humans. We have identified unexpected and large variations in plasma Lp(a) levels during renal disease, HIV-infection and in sepsis. Moreover, we have observed an association between Lp(a) and Alzheimer disease. Taken together, our observations suggest that Lp(a) may constitute a novel target in our fight against cardiovascular and neurodegenerative disorders.

The origins and impact of primate segmental duplications

Duplicated sequences are substrates for the emergence of new genes and are an important source of genetic instability associated with rare and common diseases. Analyses of primate genomes have shown an increase in the proportion of interspersed segmental duplications (SDs) within the genomes of humans and great apes. This contrasts with other mammalian genomes that seem to have their recently duplicated sequences organized in a tandem configuration. In this review, we focus on the mechanistic origin and impact of this difference with respect to evolution, genetic diversity and primate phenotype. Although many genomes will be sequenced in the future, resolution of this aspect of genomic architecture still requires high quality sequences and detailed analyses.