Primate Lineage Research Articles

Linguistic law-like compression strategies emerge to maximize coding efficiency in marmoset vocal communication.

Human language follows statistical regularities or linguistic laws. For instance, Zipf's law of brevity states that the more frequently a word is used, the shorter it tends to be. All human languages adhere to this word structure. However, it is unclear whether Zipf's law emerged de novo in humans or whether it also exists in the non-linguistic vocal systems of our primate ancestors. Using a vocal conditioning paradigm, we examined the capacity of marmoset monkeys to efficiently encode vocalizations. We observed that marmosets adopted vocal compression strategies at three levels: (i) increasing call rate, (ii) decreasing call duration and (iii) increasing the proportion of short calls. Our results demonstrate that marmosets, when able to freely choose what to vocalize, exhibit vocal statistical regularities consistent with Zipf's law of brevity that go beyond their context-specific natural vocal behaviour. This suggests that linguistic laws emerged in non-linguistic vocal systems in the primate lineage.

A Glimpse Into India’s Palaeoanthropological Past: Fossil Primates of the Pliocene and the Pleistocene

The Pliocene was a period of major faunal shift in India as older primate lineages slowly went extinct, leaving the niches vacant for cercopithecoids, specifically cercopithecids (Old World monkeys), to occupy. Among them, Presbytis sivalensis, Macaca palaeindica and Procynocephalus subhimalayanus are important, as they are potential kin to many of the South Asian and Southeast Asian monkeys living today. Further in the Pleistocene, as ecology shifted to a more grassland environment, primates such as Theropithecus delsoni and the first people of Homo sp. migrated into the subcontinent and occupied central India. All of these primate fossils are known only from a handful of fragmentary fossil remains. This article aims to discuss the discovery of fossils and the nature of these fossils from the Pliocene and the Pleistocene. Information regarding the phylogenetic affinities of these fossil primates is sporadic as well. There is a need to learn more about these primates by reanalysing existing discoveries and conducting further research into the lives of these primates of a bygone era. Such research, using modern tools and methods, will surely make significant contributions to palaeoanthropology.

Integrative omics reveals rapidly evolving regulatory sequences driving primate brain evolution.

Although continual expansion of the brain during primate evolution accounts for our enhanced cognitive capabilities, the drivers of brain evolution have scarcely been explored in these ancestral nodes. Here we performed large-scale comparative genomic, transcriptomic and epigenomic analyses to investigate the evolutionary alterations acquired by brain genes, and provide comprehensive listings of innovatory genetic elements along the evolutionary path from ancestral primates to human. The regulatory sequences associated with brain-expressed genes experienced rapid change, particularly in the ancestor of the Simiiformes. Extensive comparisons of single cell and bulk transcriptomic data between primate and non-primate brains revealed that these regulatory sequences may drive the high expression of certain genes in primate brains. Employing in utero electroporation into mouse embryonic cortex, we show that the primate-specific brain-biased gene BMP7 was recruited, probably in the ancestor of the Simiiformes, to regulate neuronal proliferation in the primate ventricular zone. Our study provides a comprehensive listing of genes and regulatory changes along the brain evolution lineage of ancestral primates leading to human. These data should be invaluable for future functional studies that will deepen our understanding not only of the genetic basis of human brain evolution but also of inherited disease.

Crows flexibly apply statistical inferences based on previous experience

Statistical inference, the ability to use limited information to draw conclusions about the likelihood of an event, is critical for decision-making during uncertainty. The ability to make statistical inferences was thought to be a uniquely human skill requiring verbal instruction and mathematical reasoning.1 However, basic inferences have been demonstrated in both preliterate and pre-numerate individuals,2,3,4,5,6,7 as well as non-human primates.8 More recently, the ability to make statistical inferences has been extended to members outside of the primate lineage in birds.9,10 True statistical inference requires subjects use relative rather than absolute frequency of previously experienced events. Here, we show that crows can relate memorized reward probabilities to infer reward-maximizing decisions. Two crows were trained to associate multiple reward probabilities ranging from 10% to 90% to arbitrary stimuli. When later faced with the choice between various stimulus combinations, crows retrieved the reward probabilities associated with individual stimuli from memory and used them to gain maximum reward. The crows showed behavioral distance and size effects when judging reward values, indicating that the crows represented probabilities as abstract magnitudes. When controlling for absolute reward frequency, crows still made reward-maximizing choices, which is the signature of true statistical inference. Our study provides compelling evidence of decision-making by relative reward frequency in a statistical inference task.

Early euprimates already had a diverse locomotor repertoire: Evidence from ankle bone morphology

The morphological adaptations of euprimates have been linked to their origin and early evolution in an arboreal environment. However, the ancestral and early locomotor repertoire of this group remains contentious. Although some tarsal bones like the astragalus and the calcaneus have been thoroughly studied, the navicular remains poorly studied despite its potential implications for foot mobility. Here, we evaluate early euprimate locomotion by assessing the shape of the navicular—an important component of the midtarsal region of the foot—using three-dimensional geometric morphometrics in relation to quantified locomotor repertoire in a wide data set of extant primates. We also reconstruct the locomotor repertoire of representatives of the major early primate lineages with a novel phylogenetically informed discriminant analysis and characterize the changes that occurred in the navicular during the archaic primate–euprimate transition. To do so, we included in our study an extensive sample of naviculars (36 specimens) belonging to different species of adapiforms, omomyiforms, and plesiadapiforms. Our results indicate that navicular shape embeds a strong functional signal, allowing us to infer the type of locomotion of extinct primates. We demonstrate that early euprimates displayed a diverse locomotor behavior, although they did not reach the level of specialization of some living forms. Finally, we show that the navicular bone experienced substantial reorganization throughout the archaic primate–euprimate transition, supporting the major functional role of the tarsus during early primate evolution. This study demonstrates that navicular shape can be used as a reliable proxy for primate locomotor behavior. In addition, it sheds light on the diverse locomotor behavior of early primates as well as on the archaic primate–euprimate transition, which involved profound morphological changes within the tarsus, including the navicular bone.

Phylogenomic analyses provide insights into primate evolution.

Comparative analysis of primate genomes within a phylogenetic context is essential for understanding the evolution of human genetic architecture and primate diversity. We present such a study of 50 primate species spanning 38 genera and 14 families, including 27 genomes first reported here, with many from previously less well represented groups, the New World monkeys and the Strepsirrhini. Our analyses reveal heterogeneous rates of genomic rearrangement and gene evolution across primate lineages. Thousands of genes under positive selection in different lineages play roles in the nervous, skeletal, and digestive systems and may have contributed to primate innovations and adaptations. Our study reveals that many key genomic innovations occurred in the Simiiformes ancestral node and may have had an impact on the adaptive radiation of the Simiiformes and human evolution.

Lineage-specific accelerated sequences underlying primate evolution.

Understanding the mechanisms underlying phenotypic innovation is a key goal of comparative genomic studies. Here, we investigated the evolutionary landscape of lineage-specific accelerated regions (LinARs) across 49 primate species. Genomic comparison with dense taxa sampling of primate species significantly improved LinAR detection accuracy and revealed many novel human LinARs associated with brain development or disease. Our study also yielded detailed maps of LinARs in other primate lineages that may have influenced lineage-specific phenotypic innovation and adaptation. Functional experimentation identified gibbon LinARs, which could have participated in the developmental regulation of their unique limb structures, whereas some LinARs in the Colobinae were associated with metabolite detoxification which may have been adaptive in relation to their leaf-eating diet. Overall, our study broadens knowledge of the functional roles of LinARs in primate evolution.

Eighty million years of rapid evolution of the primate Y chromosome.

The Y chromosome usually plays a critical role in determining male sex and comprises sequence classes that have experienced unique evolutionary trajectories. Here we generated 19 new primate sex chromosome assemblies, analysed them with 10 existing assemblies and report rapid evolution of the Y chromosome across primates. The pseudoautosomal boundary has shifted at least six times during primate evolution, leading to the formation of a Simiiformes-specific evolutionary stratum and to the independent start of young strata in Catarrhini and Platyrrhini. Different primate lineages experienced different rates of gene loss and structural and chromatin change on their Y chromosomes. Selection on several Y-linked genes has contributed to the evolution of male developmental traits across the primates. Additionally, lineage-specific expansions of ampliconic regions have further increased the diversification of the structure and gene composition of the Y chromosome. Overall, our comprehensive analysis has broadened our knowledge of the evolution of the primate Y chromosome.

Scleral appearance is not a correlate of domestication in mammals

Numerous hypotheses try to explain the unusual appearance of the human eye with its bright sclera and transparent conjunctiva and how it could have evolved from a dark-eyed phenotype, as is present in many non-human primates. Recently, it has been argued that pigmentation defects induced by self-domestication may have led to bright-eyed ocular phenotypes in humans and some other primate lineages, such as marmosets. However, it has never been systematically studied whether actual domesticated mammals consistently deviate from wild mammals in regard to their conjunctival pigmentation and if this trait might therefore be part of a domestication syndrome. Here, we test this idea by drawing phylogenetically informed comparisons from a photographic dataset spanning 13 domesticated mammal species and their closest living wild relatives (n ≥ 15 photos per taxon). We did not recover significant differences in scleral appearance or irido-scleral contrast between domesticated and wild forms, suggesting that conjunctival depigmentation, unlike cutaneous pigmentation disorders, is not a general correlate of domestication. Regardless of their domestication status, macroscopically depigmented conjunctivae were observed in carnivorans and lagomorphs, whereas ungulates generally displayed darker eyes. For some taxa, we observed pronounced intraspecific variation, which should be addressed in more exhaustive future studies. Based on our dataset, we also present preliminary evidence for a general increase of conjunctival pigmentation with eye size in mammals. Our findings suggest that conjunctival depigmentation in humans is not a byproduct of self-domestication, even if we assume that our species has undergone such a process in its recent evolutionary history.

Primate sympatry shapes the evolution of their brain architecture

The main hypotheses on the evolution of animal cognition emphasise the role of conspecifics in affecting the socio-ecological environment shaping cognition. Yet, space is often simultaneously occupied by multiple species from the same ecological guild. These sympatric species can compete for food, which may thereby stimulate or hamper cognition. Considering brain size as a proxy for cognition, we tested whether species sympatry impacted the evolution of cognition in frugivorous primates. We first retraced the evolutionary history of sympatry between frugivorous primate lineages. We then fitted phylogenetic models of the evolution of the size of several brain regions in frugivorous primates, considering or not species sympatry. We found that the evolution of the whole brain or brain regions used in immediate information processing was best fitted with models not considering sympatry. By contrast, models considering species sympatry best predicted the evolution of brain regions related to long-term memory of interactions with the socio-ecological environment, with a decrease in their size the higher the sympatry. We speculate that species sympatry, by generating intense food depletion, might lead to an over-complexification of resource spatiotemporality that counteracts the benefits of high cognitive abilities and/or might drive niche partitioning and specialisation, thereby inducing lower brain region sizes. In addition, we reported that primate species in sympatry diversify more slowly. This comparative study suggests that species sympatry significantly contributes to shaping primate evolution.

Identification and Characterization of the HERV-K (HML-8) Group of Human Endogenous Retroviruses in the Genome.

Human endogenous retroviruses (HERVs) can be vertically transmitted in a Mendelian fashion, are stably maintained in the human genome, and are estimated to constitute ∼8% of the genome. HERVs affect human physiology and pathology through their provirus-encoded protein or long terminal repeat (LTR) element effect. Characterization of the genomic distribution is an essential step to understanding the relationships between endogenous retrovirus expression and diseases. However, the poor characterization of human MMTV-like (HML)-8 prevents a detailed understanding of the regulation of the expression of this family in humans and its impact on the host genome. In light of this, the definition of an accurate and updated HERV-K HML-8 genomic map is urgently needed. In this study, we report the results of a comprehensive analysis of HERV-K HML-8 sequence presence and distribution within the human genome and hominoids, with a detailed description of the different structural and phylogenetic aspects characterizing the group. A total of 40 proviruses and 5 solo LTR elements for human were characterized, which included a detailed description of provirus structure, integration time, potentially regulated genes, transcription factor-binding sites, and primer-binding site features. Besides, 9 chimpanzee sequences, 8 gorilla sequences, and 10 orangutan sequences belonging to the HML-8 subgroup were identified. The integration time results showed that the HML-8 elements were integrated into the primate lineage around 35 and 42 million years ago (mya), during primates evolutionary speciation. Overall, the results clarified the composition of the HML-8 groups, providing an exhaustive background for subsequent functional studies.

Macroevolutionary drivers of brain evolution in primates

The main hypotheses on the evolution of animal cognition emphasise the role of conspecifics in affecting the socio-ecological environment shaping cognition. Yet, space is often simultaneously occupied by multiple species from the same ecological guild. These sympatric species can compete for food, which may thereby stimulate or hamper cognition. Considering brain size as a proxy for cognition, we tested whether species sympatry impacted the evolution of cognition in frugivorous primates. We first retraced the evolutionary history of sympatry between frugivorous primate lineages. We then fitted phylogenetic models of the evolution of the size of several brain regions in frugivorous primates, considering or not species sympatry. We found that the evolution of the whole brain or brain regions used in immediate information processing was best fitted with models not considering sympatry. By contrast, models considering species sympatry best predicted the evolution of brain regions related to long-term memory of interactions with the socio-ecological environment, with a decrease in their size the higher the sympatry. We speculate that species sympatry, by generating intense food depletion, might lead to an over-complexification of resource spatiotemporality that counteracts the benefits of high cognitive abilities and/or might drive niche partitioning and specialisation, thereby inducing lower brain region sizes. In addition, we reported that primate species in sympatry diversify more slowly. This comparative study suggests that species sympatry significantly contributes to shaping primate evolution.

Sourcing high tissue quality brains from deceased wild primates with known socio‐ecology

Abstract The selection pressures that drove dramatic encephalisation processes through the mammal lineage remain elusive, as does knowledge of brain structure reorganisation through this process. In particular, considerable structural brain changes are present across the primate lineage, culminating in the complex human brain that allows for unique behaviours such as language and sophisticated tool use. To understand this evolution, a diverse sample set of humans' closest relatives with varying socio‐ecologies is needed. However, current brain banks predominantly curate brains from primates that died in zoological gardens. We try to address this gap by establishing a field pipeline mitigating the challenges associated with brain extractions of wild primates in their natural habitat. The success of our approach is demonstrated by our ability to acquire a novel brain sample of deceased primates with highly variable socio‐ecological exposure and a particular focus on wild chimpanzees. Methods in acquiring brain tissue from wild settings are comprehensively explained, highlighting the feasibility of conducting brain extraction procedures under strict biosafety measures by trained veterinarians in field sites. Brains are assessed at a fine‐structural level via high‐resolution MRI and state‐of‐the‐art histology. Analyses confirm that excellent tissue quality of primate brains sourced in the field can be achieved with a comparable tissue quality of brains acquired from zoo‐living primates. Our field methods are noninvasive, here defined as not harming living animals, and may be applied to other mammal systems than primates. In sum, the field protocol and methodological pipeline validated here pose a major advance for assessing the influence of socio‐ecology on medium to large mammal brains, at both macro‐ and microstructural levels as well as aiding with the functional annotation of brain regions and neuronal pathways via specific behaviour assessments.

Species-specific self-DNA detection mechanisms by mammalian cyclic GMP-AMP synthases.

The mechanisms by which innate immune receptors mediate self-nonself discrimination are unclear. In this study, we found species-specific molecular determinants of self-DNA reactivity by cyclic guanosine monophosphate-adenosine monophosphate (GMP-AMP) synthase (cGAS). Human cGAS contained a catalytic domain that was intrinsically self-DNA reactive and stimulated interferon responses in diverse cell types. This reactivity was prevented by an upstream amino (N)-terminal domain. The cGAS proteins from several nonhuman primate species exhibited a similar pattern of self-DNA reactivity in cells, but chimpanzee cGAS was inactive even when its amino-terminal domain was deleted. In contrast, the N terminus of mouse cGAS promoted self-DNA reactivity. When expressed within tumors, only self-DNA-reactive cGAS proteins protected mice from tumor-induced lethality. In vitro studies of DNA- or chromatin-induced cGAS activation did not reveal species-specific activities that correlate with self-DNA reactivity observed in macrophages. Cell biological analysis revealed that self-DNA reactivity by human cGAS, but not mouse cGAS, correlated with localization to mitochondria. We found that epitope tag positions affected self-DNA reactivity in cells and that DNA present in cell lysates undermines the reliability of cGAS biochemical fractionations. These studies reveal species-specific diversity of cGAS functions, even within the primate lineage, and highlight experimental considerations for the study of this innate immune receptor.

To what extent are call combinations in chimpanzees comparable to syntax in humans?

Syntax is considered a key feature distinguishing human language from other non-human animal communication systems. However, evidence for combinatorial capacities in a wide variety of species, such as birds and monkeys, has challenged this assumption. Nevertheless, a contentious debate surrounding the evolutionary origins of syntax remains, specifically whether the combinatorial capacities displayed in animals merely illustrate a case of convergent evolution or whether it could also represent, within the primate lineage, a homologous trait to syntax in humans. In this piece, I review the literature on combinatorial signalling in our closest-living relative, the chimpanzee (Pan troglotytes), central to demonstrating a more ancient evolutionary account of syntax. Specifically, I detail the combinatorial structures highlighted in chimpanzees, the experimental evidence pointing toward the syntactic-like nature of these combinations, as well as the limitations the field needs to overcome to go a step further and address the question of the evolution of syntax more holistically. I discuss future directions building on exciting recent evidence for combinatorial flexibility in chimpanzees and the potential for learning. Finally, by proposing a compositional analysis to documented combinations of gestures with facial expressions, I argue that a promising avenue for the study of the evolution of syntax lies in the understanding of multimodal combinatorial signalling in our closest-living relatives and its ontogeny.

Evolutionary analysis of endogenous intronic retroviruses in primates reveals an enrichment in transcription binding sites associated with key regulatory processes.

Endogenous retroviruses (ERVs) are the result of the integration of retroviruses into host DNA following germline infection. Endogenous retroviruses are made up of three main genes: gag, pol, and env, each of which encodes viral proteins that can be conserved or not. ERVs have been observed in a wide range of vertebrate genomes and their functions are associated with viral silencing and gene regulation. In this work, we studied the evolutionary history of endogenous retroviruses associated with five human genes (INPP5B, DET1, PSMA1, USH2A, and MACROD2), which are located within intron sections. To verify the retroviral origin of the candidates, several approaches were used to detect and locate ERV elements. Both orthologous and paralogous genes were identified by Ensembl and then analyzed for ERV presence using RetroTector. A phylogenetic tree was reconstructed to identify the minimum time point of ERV acquisition. From that search, we detected ERVs throughout the primate lineage and in some other groups. Also, we identified the minimum origin of the ERVs from the parvorder Catarrhini to the Homininae subfamily. With the data collected, and by observing the transcription factors annotated inside ERVs, we propose that these elements play a relevant role in gene expression regulation and they probably possess important features for tumorigenesis control.

The origin and loss of interferon regulatory factor 10 (IRF10) in different lineages of vertebrates

The vertebrate IFN regulatory factor (IRF) family consists of 11 members that exert distinct roles in a variety of biological processes, including antiviral defense, regulation of cell proliferation, differentiation and apoptosis. Of these, IRF10 is widely present in different vertebrate lineages, but appears to have been lost in primates and rodents. To understand the evolutionary occurrence of IRF10, we performed comparative analyses of currently available genomic data in a taxonomically diverse set of vertebrates, and found that IRF10 originated after the divergence of chondrichthyans from gnathostomes. Phylogenetically, vertebrate IRF10 is much more closely related to IRF4 than to IRF8 or IRF9, although these four IRFs may have a common ancestor. In addition, the loss of IRF10 in Euarchontoglires might be resulted from mutation accumulation, and the rate of mutations in rodents appears to be higher than in the primate lineage. In primates, the gene-disruptive mutations may have occurred at least prior to the separation of new world monkey and old world primates, roughly 40 million years ago. Overall, we propose a detailed evolutionary scenario for IRF10, which may help us understand the evolutionary mechanisms in the expansion and contraction of the IRF family.

Cerebral Activity in Female Baboons (Papio anubis) During the Perception of Conspecific and Heterospecific Agonistic Vocalizations: a Functional Near Infrared Spectroscopy Study

The “voice areas” in the superior temporal cortex have been identified in both humans and non-human primates as selective to conspecific vocalizations only (i.e., expressed by members of our own species), suggesting its old evolutionary roots across the primate lineage. With respect to non-human primate species, it remains unclear whether the listening of vocal emotions from conspecifics leads to similar or different cerebral activations when compared to heterospecific calls (i.e., expressed by another primate species) triggered by the same emotion. Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy, the present study investigated in three lightly anesthetized female baboons (Papio anubis), temporal cortex activities during exposure to agonistic vocalizations from conspecifics and from other primates (chimpanzees—Pan troglodytes), and energy matched white noises in order to control for this low-level acoustic feature. Permutation test analyses on the extracted OxyHemoglobin signal revealed great inter-individual differences on how conspecific and heterospecific vocal stimuli were processed in baboon brains with a cortical response recorded either in the right or the left temporal cortex. No difference was found between emotional vocalizations and their energy-matched white noises. Despite the phylogenetic gap between Homo sapiens and African monkeys, modern humans and baboons both showed a highly heterogeneous brain process for the perception of vocal and emotional stimuli. The results of this study do not exclude that old evolutionary mechanisms for vocal emotional processing may be shared and inherited from our common ancestor.

A partial duplication of an X-linked gene exclusive of a primate lineage (Macaca)

Gene duplication plays a significant role in evolution. Paralogous gene copies may be lost due to the successive accumulation of deleterious mutations or remain active in the genome. In this work, a partial duplication of an X-linked region in the Macaca genus is identified and explored. Genomic comparisons reveal that the duplication encompasses the genes encoding ornithine transcarbamylase (OTC) and retinitis pigmentosa GTPase regulator (RPGR), spanning over 0.1 Mb on the chromosome 9 of Macaca. According to our analyses, the duplicated region of chromosome 9 involves partial coding sequences of both OTC and RPGR genes. Analyses of the selective pressures did not reveal significant differences in the ratio between nonsynonymous and synonymous mutations (w<1), suggesting that no selective pressures were acting in the evolutionary process. Reports for a biological role regarding some partial duplications exist in the literature, therefore, although being rare events, partial duplications of functionally important genes are worthy of study so that their impact can be explored.

Cebidae Alu Element Alignments and a Complex Non-Human Primate Radiation.

Simple SummaryRelationships among the small monkeys living in the Americas such as the squirrel monkeys, owl monkeys (the ‘night monkeys’), marmosets and capuchins (the ‘organ grinder’ monkeys) are still under debate. This study utilized multi-species DNA sequence alignments to investigate these relationships. Each alignment contained a unique Alu element insertion, a genetic marker considered ‘identical by descent’ such that the absence of the Alu element is the ancestral state. Alu element diversity reveals that the emergence and radiation of these different primate lineages was rapid and complex. The close relationship between squirrel monkey and capuchins was confirmed while the placement of owl monkey with respect to the marmoset remains unresolved. The results of this study will assist in research and conservation strategies for America’s monkeys.Phylogenetic relationships among Cebidae species of platyrrhine primates are presently under debate. Studies prior to whole genome sequence (WGS) availability utilizing unidirectional Alu repeats linked Callithrix and Saguinus as sister taxa, based on a limited number of genetic markers and specimens, while the relative positions of Cebus, Saimiri and Aotus remained controversial. Multiple WGS allowed computational detection of Alu-genome junctions, however random mutation and evolutionary decay of these short-read segments prevented phylogenetic resolution. In this study, WGS for four Cebidae genomes of marmoset, squirrel monkey, owl monkey and capuchin were analyzed for full-length Alu elements and each locus was compared to the other three genomes in all possible combinations using orthologous region sequence alignments. Over 2000 candidates were aligned and subjected to visual inspection. Approximately 34% passed inspection and were considered shared in their respective category, 48% failed due to the target being present in all four genomes, having N’s in the sequence or other sequence quality anomalies, and 18% were determined to represent near parallel insertions (NP). Wet bench locus specific PCR confirmed the presence of shared Alu insertions in all phylogenetically informative categories, providing evidence of extensive incomplete lineage sorting (ILS) and an abundance of Alu proliferation during the complex radiation of Cebidae taxa.