Hominid Lineage Research Articles

Morphological integration in the hominid midfoot

The calculation of morphological integration across living apes and humans may provide important insights into the potential influence of integration on evolutionary trajectories in the hominid lineage. Here, we quantify magnitudes of morphological integration among and within elements of the midfoot in great apes and humans to examine the link between locomotor differences and trait covariance. We test the hypothesis that the medial elements of the great ape foot are less morphologically integrated with one another compared to humans based on their abducted halluces, and aim to determine how adaptations for midfoot mobility/stiffness and locomotor specialization influence magnitudes of morphological integration. The study sample is composed of all cuneiforms, the navicular, the cuboid, and metatarsals 1–5 of Homo sapiens (n = 80), Pan troglodytes (n = 63), Gorilla gorilla (n = 39), and Pongo sp. (n = 41). Morphological integration was quantified using the integration coefficient of variation of interlandmark distances organized into sets of a priori-defined modules. Magnitudes of integration across these modules were then compared against sets of random traits from the whole midfoot. Results show that all nonhuman apes have less integrated medial elements, whereas humans have highly integrated medial elements, suggesting a link between hallucal abduction and reduced levels of morphological integration. However, we find considerable variation in magnitudes of morphological integration across metatarsals 2–5, the intermediate and lateral cuneiform, the cuboid, and navicular, emphasizing the influence of functional and nonfunctional factors in magnitudes of integration. Lastly, we find that humans and orangutans show the lowest overall magnitudes of integration in the midfoot, which may be related to their highly specialized functions, and suggest a link between strong diversifying selection and reduced magnitudes of morphological integration.

If Skill is Normative, Then Norms are Everywhere

Abstract Birch sketches out an ingenious account of how the psychology of social norms emerged from individual-level norms of skill. We suggest that these individual-level norms of skill are likely to be much more widespread than Birch suggests, extending deeper into the hominid lineage, across modern great ape species, all the way to distantly related creatures like honeybees. This suggests that there would have been multiple opportunities for social norms to emerge from skill norms in human prehistory.

Joint Action without Mutual Beliefs

Abstract Joint action among human beings is characterized by using elaborate cognitive feats, such as representing the mental states of others about a certain state of affairs. It is still debated how these capacities evolved in the hominid lineage. I suggest that the consolidation of a shared practice over time can foster the predictability of other’s behavior. This might facilitate the evolutionary passage from inferring what others might know by simply seeing them and what they are viewing towards a mutual awareness of each other’s beliefs. I will examine the case for cooperative hunting in one chimpanzee community and argue that it is evidence that they have the potential to achieve common ground, suggesting that the consolidation of a practice might have supported the evolution of higher social cognition in the hominid lineage.

Genomic Variation, Evolvability, and the Paradox of Mental Illness.

Twentieth-century genetics was hard put to explain the irregular behavior of neuropsychiatric disorders. Autism and schizophrenia defy a principle of natural selection; they are highly heritable but associated with low reproductive success. Nevertheless, they persist. The genetic origins of such conditions are confounded by the problem of variable expression, that is, when a given genetic aberration can lead to any one of several distinct disorders. Also, autism and schizophrenia occur on a spectrum of severity, from mild and subclinical cases to the overt and disabling. Such irregularities reflect the problem of missing heritability; although hundreds of genes may be associated with autism or schizophrenia, together they account for only a small proportion of cases. Techniques for higher resolution, genomewide analysis have begun to illuminate the irregular and unpredictable behavior of the human genome. Thus, the origins of neuropsychiatric disorders in particular and complex disease in general have been illuminated. The human genome is characterized by a high degree of structural and behavioral variability: DNA content variation, epistasis, stochasticity in gene expression, and epigenetic changes. These elements have grown more complex as evolution scaled the phylogenetic tree. They are especially pertinent to brain development and function. Genomic variability is a window on the origins of complex disease, neuropsychiatric disorders, and neurodevelopmental disorders in particular. Genomic variability, as it happens, is also the fuel of evolvability. The genomic events that presided over the evolution of the primate and hominid lineages are over-represented in patients with autism and schizophrenia, as well as intellectual disability and epilepsy. That the special qualities of the human genome that drove evolution might, in some way, contribute to neuropsychiatric disorders is a matter of no little interest.

A comparison of axial trunk rotation during bipedal walking between humans and Japanese macaques

Human walking involves out-of-phase axial rotations of the thorax and pelvis. It has long been believed that this rotational capability is a distinctive feature of the genus Homo. However, Thompson et al. (2015) showed that chimpanzees also counter-rotate their thorax relative to the pelvis during bipedal walking, which raised questions regarding the origins and development of this characteristic. In this study, we measured the axial rotation of the trunk during bipedal walking in humans and macaques to investigate if intra-trunk axial rotations are observed in non-hominoid primate species. We collected three-dimensional trunk kinematic data during bipedal walking in six humans and five Japanese macaques. The human subjects walked on a treadmill, and the animal subjects walked on a 5-m runway. During walking, the positions of cluster markers, which defined trunk segments, were recorded by multiple video cameras. Segmental xyz coordinates were digitized, and transverse rotations were calculated using motion analysis software. Although trunk rotations in the global coordinate system were greater in macaques than in humans, the intra-trunk rotation and range of motion showed a similar pattern in the two species. Thoracic rotation relative to the pelvis during bipedal walking is not unique to the hominid lineage but rather a characteristic generated by the mechanical requirements of bipedal walking. The fact that the range of motion of counter rotation is similar in these species infers that an optimal range of rotation exists for bipedal walking.

Molecular and cellular evolution of corticogenesis in amniotes.

The cerebral cortex varies dramatically in size and complexity between amniotes due to differences in neuron number and composition. These differences emerge during embryonic development as a result of variations in neurogenesis, which are thought to recapitulate modifications occurred during evolution that culminated in the human neocortex. Here, we review work from the last few decades leading to our current understanding of the evolution of neurogenesis and size of the cerebral cortex. Focused on specific examples across vertebrate and amniote phylogeny, we discuss developmental mechanisms regulating the emergence, lineage, complexification and fate of cortical germinal layers and progenitor cell types. At the cellular level, we discuss the fundamental impact of basal progenitor cells and the advent of indirect neurogenesis on the increased number and diversity of cortical neurons and layers in mammals, and on cortex folding. Finally, we discuss recent work that unveils genetic and molecular mechanisms underlying this progressive expansion and increased complexity of the amniote cerebral cortex during evolution, with a particular focus on those leading to human-specific features. Whereas new genes important in human brain development emerged the recent hominid lineage, regulation of the patterns and levels of activity of highly conserved signaling pathways are beginning to emerge as mechanisms of central importance in the evolutionary increase in cortical size and complexity across amniotes.

Two to Tango: Co-evolution of Hominid Natural Killer Cell Receptors and MHC.

Natural killer (NK) cells have diverse roles in hominid immunity and reproduction. Modulating these functions are the interactions between major histocompatibility complex (MHC) class I molecules that are ligands for two NK cell surface receptor types. Diverse killer cell immunoglobulin-like receptors (KIR) bind specific motifs encoded within the polymorphic MHC class I cell surface glycoproteins, while, in more conserved interactions, CD94:NKG2A receptors recognize MHC-E with bound peptides derived from MHC class I leader sequences. The hominid lineage presents a choreographed co-evolution of KIR with their MHC class I ligands. MHC-A, -B, and -C are present in all great apes with species-specific haplotypic variation in gene content. The Bw4 epitope recognized by lineage II KIR is restricted to MHC-B but also present on some gorilla and human MHC-A. Common to great apes, but rare in humans, are MHC-B possessing a C1 epitope recognized by lineage III KIR. MHC-C arose from duplication of MHC-B and is fixed in all great apes except orangutan, where it exists on approximately 50% of haplotypes and all allotypes are C1-bearing. Recent study showed that gorillas possess yet another intermediate MHC organization compared to humans. Like orangutans, but unlike the Pan-Homo species, duplication of MHC-B occurred. However, MHC-C is fixed, and the MHC-C C2 epitope (absent in orangutans) emerges. The evolution of MHC-C drove expansion of its cognate lineage III KIR. Recently, position −21 of the MHC-B leader sequence has been shown to be critical in determining NK cell educational outcome. In humans, methionine (−21M) results in CD94:NKG2A-focused education whereas threonine (−21T) produces KIR-focused education. This is another dynamic position among hominids. Orangutans have exclusively −21M, consistent with their intermediate stage in lineage III KIR-focused evolution. Gorillas have both −21M and −21T, like humans, but they are unequally encoded by their duplicated B genes. Chimpanzees have near-fixed −21T, indicative of KIR-focused NK education. Harmonious with this observation, chimpanzee KIR exhibit strong binding and, compared to humans, smaller differences between binding levels of activating and inhibitory KIR. Consistent between these MHC-NK cell receptor systems over the course of hominid evolution is the evolution of polymorphism favoring the more novel and dynamic KIR system.

Cerebral torque is human specific and unrelated to brain size

The term “cerebral torque” refers to opposing right–left asymmetries of frontal and parieto-occipital regions. These are assumed to derive from a lateralized gradient of embryological development of the human brain. To establish the timing of its evolution, we computed and compared the torque, in terms of three principal features, namely petalia, shift, and bending of the inter-hemispheric fissure as well as the inter-hemispheric asymmetry of brain length, height and width for in vivo Magnetic Resonance Imaging (MRI) scans of 91 human and 78 chimpanzee brains. We found that the cerebral torque is specific to the human brain and that its magnitude is independent of brain size and that it comprises features that are inter-related. These findings are consistent with the concept that a “punctuational” genetic change of relatively large effect introduced lateralization in the hominid lineage. The existence of the cerebral torque remains an unsolved mystery and the present study provides further support for this most prominent structural brain asymmetry being specific to the human brain. Establishing the genetic origins of the torque may, therefore, have relevance for a better understanding on human evolution, the organisation of the human brain, and, perhaps, also aspects of the neural basis of language.

A polymorphic residue that attenuates the antiviral potential of interferon lambda 4 in hominid lineages.

As antimicrobial signalling molecules, type III or lambda interferons (IFNλs) are critical for defence against infection by diverse pathogens, including bacteria, fungi and viruses. Counter-intuitively, expression of one member of the family, IFNλ4, is associated with decreased clearance of hepatitis C virus (HCV) in the human population; by contrast, a natural frameshift mutation that abrogates IFNλ4 production improves HCV clearance. To further understand how genetic variation between and within species affects IFNλ4 function, we screened a panel of all known extant coding variants of human IFNλ4 for their antiviral potential and identify three that substantially affect activity: P70S, L79F and K154E. The most notable variant was K154E, which was found in African Congo rainforest ‘Pygmy’ hunter-gatherers. K154E greatly enhanced in vitro activity in a range of antiviral (HCV, Zika virus, influenza virus and encephalomyocarditis virus) and gene expression assays. Remarkably, E154 is the ancestral residue in mammalian IFNλ4s and is extremely well conserved, yet K154 has been fixed throughout evolution of the hominid genus Homo, including Neanderthals. Compared to chimpanzee IFNλ4, the human orthologue had reduced activity due to amino acid K154. Comparison of published gene expression data from humans and chimpanzees showed that this difference in activity between K154 and E154 in IFNλ4 correlates with differences in antiviral gene expression in vivo during HCV infection. Mechanistically, our data show that the human-specific K154 negatively affects IFNλ4 activity through a novel means by reducing its secretion and potency. We thus demonstrate that attenuated activity of IFNλ4 is conserved among humans and postulate that differences in IFNλ4 activity between species contribute to distinct host-specific responses to—and outcomes of—infection, such as HCV infection. The driver of reduced IFNλ4 antiviral activity in humans remains unknown but likely arose between 6 million and 360,000 years ago in Africa.

Coming like animals

The evolutionary origin of orgasm in the hominid lineage that led to Homo sapiens has given rise to numerous debates on its eventual adaptive advantages. This article takes a step sideways by exploring other branches and instances of cross-breeding in the tree of life. How do other animal species experience sexual pleasure and orgasm, with a fellow creature or … with a human? After examining the diverse representations of animal pleasure (in popular culture, art, works on artificial insemination, zoophilic pornography), the author suggests that it obliges us to reflect on the configuration and the limits of the ethical universe that we share with animals.

The Logical Problem and the Theoretician's Dilemma

The theory‐theory of human uniqueness posits that the capacity to theorize, in a way strongly analogous to theorizing in scientific practice, was a key innovation in the hominid lineage and was responsible for many of our unique cognitive traits. One of the central arguments that its proponents have used to support the claim that animals are not theorists, the logical problem, bears strong similarities to Hempel's theoretician's dilemma, which purports to show that theories are unnecessary. This similarity threatens to undermine both the claim that theorizing serves a unique, adaptive role in human cognition and our ability to test for the presence of theories. I examine two historical responses to the theoretician's dilemma and argue that they open up strategies for experimentally testing for theoretical ability in other animals.

Three Distinct Glutamate Decarboxylase Genes in Vertebrates.

Gamma-aminobutyric acid (GABA) is a widely conserved signaling molecule that in animals has been adapted as a neurotransmitter. GABA is synthesized from the amino acid glutamate by the action of glutamate decarboxylases (GADs). Two vertebrate genes, GAD1 and GAD2, encode distinct GAD proteins: GAD67 and GAD65, respectively. We have identified a third vertebrate GAD gene, GAD3. This gene is conserved in fishes as well as tetrapods. We analyzed protein sequence, gene structure, synteny, and phylogenetics to identify GAD3 as a homolog of GAD1 and GAD2. Interestingly, we found that GAD3 was lost in the hominid lineage. Because of the importance of GABA as a neurotransmitter, GAD3 may play important roles in vertebrate nervous systems.

High diversity and rapid diversification in the head louse, Pediculus humanus (Pediculidae: Phthiraptera).

The study analyzes sequence variation of two mitochondrial genes (COI, cytb) in Pediculus humanus from three countries (Egypt, Pakistan, South Africa) that have received little prior attention, and integrates these results with prior data. Analysis indicates a maximum K2P distance of 10.3% among 960 COI sequences and 13.8% among 479 cytb sequences. Three analytical methods (BIN, PTP, ABGD) reveal five concordant OTUs for COI and cytb. Neighbor-Joining analysis of the COI sequences confirm five clusters; three corresponding to previously recognized mitochondrial clades A, B, C and two new clades, “D” and “E”, showing 2.3% and 2.8% divergence from their nearest neighbors (NN). Cytb data corroborate five clusters showing that clades “D” and “E” are both 4.6% divergent from their respective NN clades. Phylogenetic analysis supports the monophyly of all clusters recovered by NJ analysis. Divergence time estimates suggest that the earliest split of P. humanus clades occured slightly more than one million years ago (MYa) and the latest about 0.3 MYa. Sequence divergences in COI and cytb among the five clades of P. humanus are 10X those in their human host, a difference that likely reflects both rate acceleration and the acquisition of lice clades from several archaic hominid lineages.

Positive selection underlies the species-specific binding of Plasmodium falciparum RH5 to human basigin.

Plasmodium falciparum, the causative agent of the deadliest form of malaria, is a member of the Laverania subgenus, which includes ape-infecting parasites. P.falciparum is thought to have originated in gorillas, although infection is now restricted to humans. Laverania parasites display remarkable host-specificity, which is partially mediated by the interaction between parasite ligands and host receptors. We analyse the evolution of BSG (basigin) and GYPA (glycophorin A) in primates/hominins, as well as of their Plasmodium-encoded ligands, PfRH5 and PfEBA175. We show that, in primates, positive selection targeted two sites in BSG (F27 and H102), both involved in PfRH5 binding. A population genetics-phylogenetics approach detected the strongest selection for the gorilla lineage: one of the positively selected sites (K191) is a major determinant of PfRH5 binding affinity. Analysis of RH5 genes indicated episodic selection on the P.falciparum branch; the positively selected W447 site is known to stabilize the interaction with human basigin. Conversely, we detect no selection in the receptor-binding region of EBA175 in the P.falciparum lineage. Its host receptor, GYPA, shows evidence of positive selection in all hominid lineages; selected codons include glycosylation sites that modulate PfEBA175 binding affinity. Data herein provide an evolutionary explanation for species-specific binding of the PfRH5-BSG ligand-receptor pair and support the hypothesis that positive selection at these genes drove the host shift leading to the emergence of P.falciparum as a human pathogen.

A one-million-year-old hominid distal ulna from Olduvai Gorge, Tanzania.

Our aim was to recover new evidence of the evolution of the hominid lineage. We undertook paleontological fieldwork at Olduvai Gorge, Tanzania, in one of the richest paleoanthropological sites in the world, documenting the evolution of our lineage and its environmental contexts over the last 2 million years. During field work in 2012, the Olduvai Vertebrate Paleontology Project discovered the distal end of a hominid ulna (OH 82) on the north side of Olduvai Gorge a few meters west of the Third Fault, eroding from Bed III sediments that are ∼1 million years in age. The size and morphology of this distal ulna falls within the normal range of variation seen in humans, although at the larger end of the distribution.

Culture, urbanism and changing human biology

Anthropologists have long known that human activity driven by culture changes the environment. This is apparent in the archeological record and through the study of the modern environment. Perhaps the largest change since the Paleolithic era is the organization of human populations in cities. New environments can reshape human biology through evolution as shown by the evolution of the hominid lineage. Evolution is not the only process capable of reshaping our biology. Some changes in our human biology are adaptive and evolutionary while others are pathological. What changes in human biology may be wrought by the modern urban environment? One significant new change in the environment is the introduction of pollutants largely through urbanization. Pollutants can affect human biology in myriad ways. Evidence shows that human growth, reproduction and cognitive functioning can be altered by some pollutants, and altered in different ways depending on the pollutant. Thus, pollutants have significance for human biologists and anthropologists generally. Further, they illustrate the bio-cultural interaction characterizing human change. Humans adapt by changing the environment, a cultural process, and then change biologically to adjust to that new environment. This ongoing, interactive process is a fundamental characteristic of human change over the millennia.

Response to ‘Fists of furry: at what point did human fists part company with the rest of the hominid lineage?’

Although it is true that hands do sometimes suffer serious injury when humans fight, epidemiology of interpersonal violence does not support the suggestion by King ([King, 2013][1]) that the fist is a fragile and ineffective weapon. In modern societies, interpersonal violence is the most frequent

Fists of furry: at what point did human fists part company with the rest of the hominid lineage?

Combat is by definition competitive. Heritable advantages in fighting ability can be expected to play significant roles in replication of contributory genes. A recent paper ([Morgan and Carrier, 2013][1]) used innovative and interesting methodology to suggest that there has been strong selection on

Lentivirus restriction by diverse primate APOBEC3A proteins

Rhesus macaque APOBEC3A (rhA3A) is capable of restricting both simian–human immunodeficiency virus (SHIVΔvif) and human immunodeficiency virus (HIV-1Δvif) to a greater extent than hA3A. We constructed chimeric A3A proteins to define the domains required for differential lentivirus restriction. Substitution of amino acids 25–33 from rhA3A into hA3A was sufficient to restrict HIVΔvif to levels similar to rhA3A restriction of SHIVΔvif. We tested if differential lentivirus restriction is conserved between A3A from Old World monkey and hominid lineages. A3A from African green monkey restricted SHIVΔvif but not HIV-1Δvif and colobus monkey A3A restricted both wild type and SHIVΔvif and HIV-1Δvif. In contrast, the gibbon ape A3A restricted neither SHIVΔvif nor HIV-1Δvif. Restriction of SHIVΔvif and HIV-1Δvif by New World monkey A3A proteins was not conserved as the A3A from the squirrel monkey but not the northern owl monkey restricted SHIVΔvif. Finally, the colobus A3A protein appears to restrict by a novel post-entry mechanism.

Evolutionary dynamism of the primate LRRC37 gene family

Core duplicons in the human genome represent ancestral duplication modules shared by the majority of intrachromosomal duplication blocks within a given chromosome. These cores are associated with the emergence of novel gene families in the hominoid lineage, but their genomic organization and gene characterization among other primates are largely unknown. Here, we investigate the genomic organization and expression of the core duplicon on chromosome 17 that led to the expansion of LRRC37 during primate evolution. A comparison of the LRRC37 gene family organization in human, orangutan, macaque, marmoset, and lemur genomes shows the presence of both orthologous and species-specific gene copies in all primate lineages. Expression profiling in mouse, macaque, and human tissues reveals that the ancestral expression of LRRC37 was restricted to the testis. In the hominid lineage, the pattern of LRRC37 became increasingly ubiquitous, with significantly higher levels of expression in the cerebellum and thymus, and showed a remarkable diversity of alternative splice forms. Transfection studies in HeLa cells indicate that the human FLAG-tagged recombinant LRRC37 protein is secreted after cleavage of a transmembrane precursor and its overexpression can induce filipodia formation.