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Science (New York, N.Y.) Oct 2023The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus...
The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.
Topics: Animals; Humans; Gene Expression Profiling; Gorilla gorilla; Hominidae; Macaca mulatta; Pan troglodytes; Phylogeny; Transcriptome; Neocortex; Species Specificity; Temporal Lobe; Cognition
PubMed: 37824638
DOI: 10.1126/science.ade9516 -
Cell Jul 2023Comparative studies of great apes provide a window into our evolutionary past, but the extent and identity of cellular differences that emerged during hominin evolution... (Comparative Study)
Comparative Study
Comparative studies of great apes provide a window into our evolutionary past, but the extent and identity of cellular differences that emerged during hominin evolution remain largely unexplored. We established a comparative loss-of-function approach to evaluate whether human cells exhibit distinct genetic dependencies. By performing genome-wide CRISPR interference screens in human and chimpanzee pluripotent stem cells, we identified 75 genes with species-specific effects on cellular proliferation. These genes comprised coherent processes, including cell-cycle progression and lysosomal signaling, which we determined to be human-derived by comparison with orangutan cells. Human-specific robustness to CDK2 and CCNE1 depletion persisted in neural progenitor cells and cerebral organoids, supporting the G1-phase length hypothesis as a potential evolutionary mechanism in human brain expansion. Our findings demonstrate that evolutionary changes in human cells reshaped the landscape of essential genes and establish a platform for systematically uncovering latent cellular and molecular differences between species.
Topics: Animals; Humans; Hominidae; Neural Stem Cells; Pan troglodytes; Pluripotent Stem Cells; Stem Cells
PubMed: 37343560
DOI: 10.1016/j.cell.2023.05.043 -
Nature Aug 2023Human-specific genomic changes contribute to the unique functionalities of the human brain. The cellular heterogeneity of the human brain and the complex regulation of...
Human-specific genomic changes contribute to the unique functionalities of the human brain. The cellular heterogeneity of the human brain and the complex regulation of gene expression highlight the need to characterize human-specific molecular features at cellular resolution. Here we analysed single-nucleus RNA-sequencing and single-nucleus assay for transposase-accessible chromatin with sequencing datasets for human, chimpanzee and rhesus macaque brain tissue from posterior cingulate cortex. We show a human-specific increase of oligodendrocyte progenitor cells and a decrease of mature oligodendrocytes across cortical tissues. Human-specific regulatory changes were accelerated in oligodendrocyte progenitor cells, and we highlight key biological pathways that may be associated with the proportional changes. We also identify human-specific regulatory changes in neuronal subtypes, which reveal human-specific upregulation of FOXP2 in only two of the neuronal subtypes. We additionally identify hundreds of new human accelerated genomic regions associated with human-specific chromatin accessibility changes. Our data also reveal that FOS::JUN and FOX motifs are enriched in the human-specifically accessible chromatin regions of excitatory neuronal subtypes. Together, our results reveal several new mechanisms underlying the evolutionary innovation of human brain at cell-type resolution.
Topics: Animals; Humans; Cell Nucleus; Chromatin; Datasets as Topic; Evolution, Molecular; Genome, Human; Genomics; Gyrus Cinguli; Macaca mulatta; Neurons; Oligodendroglia; Pan troglodytes; Single-Cell Gene Expression Analysis; Stem Cells; Transposases; Chromatin Assembly and Disassembly
PubMed: 37468639
DOI: 10.1038/s41586-023-06338-4 -
PLoS Biology Sep 2023Human language is supported by a cortical network involving Broca's area, which comprises Brodmann Areas 44 and 45 (BA44 and BA45). While cytoarchitectonic homolog areas...
Human language is supported by a cortical network involving Broca's area, which comprises Brodmann Areas 44 and 45 (BA44 and BA45). While cytoarchitectonic homolog areas have been identified in nonhuman primates, it remains unknown how these regions evolved to support human language. Here, we use histological data and advanced cortical registration methods to precisely compare the morphology of BA44 and BA45 in humans and chimpanzees. We found a general expansion of Broca's areas in humans, with the left BA44 enlarging the most, growing anteriorly into a region known to process syntax. Together with recent functional and receptorarchitectural studies, our findings support the conclusion that BA44 evolved from an action-related region to a bipartite system, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Our findings add novel insights to the longstanding debate on the relationship between language and action, and the evolution of Broca's area.
Topics: Humans; Animals; Brain; Language; Pan troglodytes
PubMed: 37656748
DOI: 10.1371/journal.pbio.3002266 -
Dementia & Neuropsychologia 2024The purpose of this review is to highlight the most important aspects of the anatomical and functional uniqueness of the human brain. For this, a comparison is made... (Review)
Review
The purpose of this review is to highlight the most important aspects of the anatomical and functional uniqueness of the human brain. For this, a comparison is made between our brains and those of our closest ancestors (chimpanzees and bonobos) and human ancestors. During human evolution, several changes occurred in the brain, such as an absolute increase in brain size and number of cortical neurons, in addition to a greater degree of functional lateralization and anatomical asymmetry. Also, the cortical cytoarchitecture became more diversified and there was an increase in the number of intracortical networks and networks extending from the cerebral cortex to subcortical structures, with more neural networks being invested in multisensory and sensory-motor-affective-cognitive integration. These changes permitted more complex, flexible and versatile cognitive abilities and social behavior, such as shared intentionality and symbolic articulated language, which, in turn, made possible the formation of larger social groups and cumulative cultural evolution that are characteristic of our species.
PubMed: 38628563
DOI: 10.1590/1980-5764-DN-2023-0078 -
Nature May 2024Human centromeres have been traditionally very difficult to sequence and assemble owing to their repetitive nature and large size. As a result, patterns of human...
Human centromeres have been traditionally very difficult to sequence and assemble owing to their repetitive nature and large size. As a result, patterns of human centromeric variation and models for their evolution and function remain incomplete, despite centromeres being among the most rapidly mutating regions. Here, using long-read sequencing, we completely sequenced and assembled all centromeres from a second human genome and compared it to the finished reference genome. We find that the two sets of centromeres show at least a 4.1-fold increase in single-nucleotide variation when compared with their unique flanks and vary up to 3-fold in size. Moreover, we find that 45.8% of centromeric sequence cannot be reliably aligned using standard methods owing to the emergence of new α-satellite higher-order repeats (HORs). DNA methylation and CENP-A chromatin immunoprecipitation experiments show that 26% of the centromeres differ in their kinetochore position by >500 kb. To understand evolutionary change, we selected six chromosomes and sequenced and assembled 31 orthologous centromeres from the common chimpanzee, orangutan and macaque genomes. Comparative analyses reveal a nearly complete turnover of α-satellite HORs, with characteristic idiosyncratic changes in α-satellite HORs for each species. Phylogenetic reconstruction of human haplotypes supports limited to no recombination between the short (p) and long (q) arms across centromeres and reveals that novel α-satellite HORs share a monophyletic origin, providing a strategy to estimate the rate of saltatory amplification and mutation of human centromeric DNA.
Topics: Animals; Humans; Centromere; Centromere Protein A; DNA Methylation; DNA, Satellite; Evolution, Molecular; Genetic Variation; Kinetochores; Macaca; Pan troglodytes; Polymorphism, Single Nucleotide; Pongo; Male; Female; Reference Standards; Chromatin Immunoprecipitation; Haplotypes; Mutation; Gene Amplification; Sequence Alignment; Chromatin; Species Specificity
PubMed: 38570684
DOI: 10.1038/s41586-024-07278-3 -
ELife Jul 2023Inflammasomes are cytosolic innate immune complexes that assemble upon detection of diverse pathogen-associated cues and play a critical role in host defense and...
Inflammasomes are cytosolic innate immune complexes that assemble upon detection of diverse pathogen-associated cues and play a critical role in host defense and inflammatory pathogenesis. Here, we find that the human inflammasome-forming sensor CARD8 senses HIV-1 infection via site-specific cleavage of the CARD8 N-terminus by the HIV protease (HIV-1). HIV-1 cleavage of CARD8 induces pyroptotic cell death and the release of pro-inflammatory cytokines from infected cells, processes regulated by Toll-like receptor stimulation prior to viral infection. In acutely infected cells, CARD8 senses the activity of both de novo translated HIV-1 and packaged HIV-1 that is released from the incoming virion. Moreover, our evolutionary analyses reveal that the HIV-1 cleavage site in human CARD8 arose after the divergence of chimpanzees and humans. Although chimpanzee CARD8 does not recognize proteases from HIV or simian immunodeficiency viruses from chimpanzees (SIVcpz), SIVcpz does cleave human CARD8, suggesting that SIVcpz was poised to activate the human CARD8 inflammasome prior to its cross-species transmission into humans. Our findings suggest a unique role for CARD8 inflammasome activation in response to lentiviral infection of humans.
Topics: Animals; Humans; Inflammasomes; HIV-1; Pan troglodytes; HIV Infections; Simian Immunodeficiency Virus; Apoptosis Regulatory Proteins; Neoplasm Proteins; CARD Signaling Adaptor Proteins
PubMed: 37417868
DOI: 10.7554/eLife.84108 -
Nature Ecology & Evolution Sep 2023Archaic admixture has had a substantial impact on human evolution with multiple events across different clades, including from extinct hominins such as Neanderthals and...
Archaic admixture has had a substantial impact on human evolution with multiple events across different clades, including from extinct hominins such as Neanderthals and Denisovans into modern humans. In great apes, archaic admixture has been identified in chimpanzees and bonobos but the possibility of such events has not been explored in other species. Here, we address this question using high-coverage whole-genome sequences from all four extant gorilla subspecies, including six newly sequenced eastern gorillas from previously unsampled geographic regions. Using approximate Bayesian computation with neural networks to model the demographic history of gorillas, we find a signature of admixture from an archaic 'ghost' lineage into the common ancestor of eastern gorillas but not western gorillas. We infer that up to 3% of the genome of these individuals is introgressed from an archaic lineage that diverged more than 3 million years ago from the common ancestor of all extant gorillas. This introgression event took place before the split of mountain and eastern lowland gorillas, probably more than 40 thousand years ago and may have influenced perception of bitter taste in eastern gorillas. When comparing the introgression landscapes of gorillas, humans and bonobos, we find a consistent depletion of introgressed fragments on the X chromosome across these species. However, depletion in protein-coding content is not detectable in eastern gorillas, possibly as a consequence of stronger genetic drift in this species.
Topics: Animals; Humans; Gorilla gorilla; Pan paniscus; Bayes Theorem; Hominidae; Pan troglodytes; Neanderthals
PubMed: 37500909
DOI: 10.1038/s41559-023-02145-2 -
Journal of Biomechanics Aug 2023Motion analysis, as applied to evolutionary biomechanics, has experienced its own evolution over the last 50 years. Here we review how an ever-increasing fossil record,... (Review)
Review
Motion analysis, as applied to evolutionary biomechanics, has experienced its own evolution over the last 50 years. Here we review how an ever-increasing fossil record, together with continuing advancements in biomechanics techniques, have shaped our understanding of the origin of upright bipedal walking. The original, and long-established hypothesis held by Lamarck (1809), Darwin (1859) and Keith (1934), amongst others, maintained that bipedality originated in an arboreal context. However, the first field studies of gorilla and chimpanzees from the 1960's, highlighted their so-called 'knucklewalking' quadrupedalism, leading scientists to assume, semi-automatically, that knucklewalking must have been the precursor to bipedality. It would not be until the discovery of skeletons of early human relatives Australopithecus afarensis and Australopithecus prometheus, and the inclusion of methods of analysis from computer science, biomechanics, sports science and medicine, that the knucklewalking hypothesis would be most robustly challenged. Their short, but human-like lower limbs and human-like hand indicated that knucklewalking was not part of our ancestral locomotor repertoire. Rather, most current research in evolutionary biomechanics agrees it was a combination of climbing and bipedalism, both in an arboreal context, which facilitated upright, terrestrial, bipedal walking over short distances.
Topics: Animals; Humans; Biomechanical Phenomena; Walking; Pan troglodytes; Biological Evolution; Locomotion
PubMed: 37451208
DOI: 10.1016/j.jbiomech.2023.111701 -
Nature Immunology Mar 2024A nasally delivered chimpanzee adenoviral-vectored severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine (ChAd-SARS-CoV-2-S) is currently used in India...
A nasally delivered chimpanzee adenoviral-vectored severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine (ChAd-SARS-CoV-2-S) is currently used in India (iNCOVACC). Here, we update this vaccine by creating ChAd-SARS-CoV-2-BA.5-S, which encodes a prefusion-stabilized BA.5 spike protein. Whereas serum neutralizing antibody responses induced by monovalent or bivalent adenoviral vaccines were poor against the antigenically distant XBB.1.5 strain and insufficient to protect in passive transfer experiments, mucosal antibody and cross-reactive memory T cell responses were robust, and protection was evident against WA1/2020 D614G and Omicron variants BQ.1.1 and XBB.1.5 in mice and hamsters. However, depletion of memory CD8 T cells before XBB.1.5 challenge resulted in loss of protection against upper and lower respiratory tract infection. Thus, nasally delivered vaccines stimulate mucosal immunity against emerging SARS-CoV-2 strains, and cross-reactive memory CD8 T cells mediate protection against lung infection by antigenically distant strains in the setting of low serum levels of cross-reactive neutralizing antibodies.
Topics: Cricetinae; Animals; Mice; CD8-Positive T-Lymphocytes; SARS-CoV-2; COVID-19; Respiratory Tract Infections; Vaccines; Antibodies, Neutralizing; Broadly Neutralizing Antibodies; Pan troglodytes
PubMed: 38337035
DOI: 10.1038/s41590-024-01743-x