In search of the last common ancestor: new findings on wild chimpanzees

Modelling the behaviour of extinct hominins is essential in order to devise useful hypotheses of our species'' evolutionary origins for testing in the palaeontological and archaeological records. One approach is to model the last common ancestor (LCA) of living apes and humans, based on current ethological and ecological knowledge of our closest living relations. Such referential modelling is based on rigorous, ongoing field studies of the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). This paper reviews recent findings from nature, focusing on those with direct implications for hominin evolution, e.g. apes, using elementary technology to access basic resources such as food and water, or sheltering in caves or bathing as thermoregulatory adaptations. I give preference to studies that directly address key issues, such as whether stone artefacts are detectible before the Oldowan, based on the percussive technology of hammer and anvil use by living apes. Detailed comparative studies of chimpanzees living in varied habitats, from rainforest to savannah, reveal that some behavioural patterns are universal (e.g. shelter construction), while others show marked (e.g. extractive foraging) or nuanced (e.g. courtship) cross-populational variation. These findings allow us to distinguish between retained, primitive traits of the LCA versus derived ones in the human lineage.     

Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees

To study the genomic divergences among hominoids and to estimate the effective population size of the common ancestor of humans and chimpanzees, we selected 53 autosomal intergenic nonrepetitive DNA segments from the human genome and sequenced them in a human, a chimpanzee, a gorilla, and an orangutan. The average sequence divergence was only 1.24% +/- 0.07% for the human-chimpanzee pair, 1.62% +/- 0.08% for the human-gorilla pair, and 1.63% +/- 0.08% for the chimpanzee-gorilla pair. These estimates, which were confirmed by additional data from GenBank, are substantially lower than previous ones, which included repetitive sequences and might have been based on less-accurate sequence data. The average sequence divergences between orangutans and humans, chimpanzees, and gorillas were 3.08% +/- 0.11%, 3.12% +/- 0.11%, and 3.09% +/- 0.11%, respectively, which also are substantially lower than previous estimates. The sequence divergences in other regions between hominoids were estimated from extensive data in GenBank and the literature, and Alus showed the highest divergence, followed in order by Y-linked noncoding regions, pseudogenes, autosomal intergenic regions, X-linked noncoding regions, synonymous sites, introns, and nonsynonymous sites. The neighbor-joining tree derived from the concatenated sequence of the 53 segments--24,234 bp in length--supports the Homo-Pan clade with a 100% bootstrap value. However, when each segment is analyzed separately, 22 of the 53 segments (approximately 42%) give a tree that is incongruent with the species tree, suggesting a large effective population size (N(e)) of the common ancestor of Homo and Pan. Indeed, a parsimony analysis of the 53 segments and 37 protein-coding genes leads to an estimate of N(e) = 52,000 to 96,000. As this estimate is 5 to 9 times larger than the long-term effective population size of humans (approximately 10,000) estimated from various genetic polymorphism data, the human lineage apparently had experienced a large reduction in effective population size after its separation from the chimpanzee lineage. Our analysis assumes a molecular clock, which is in fact supported by the sequence data used. Taking the orangutan speciation date as 12 to 16 million years ago, we obtain an estimate of 4.6 to 6.2 million years for the Homo-Pan divergence and an estimate of 6.2 to 8.4 million years for the gorilla speciation date, suggesting that the gorilla lineage branched off 1.6 to 2.2 million years earlier than did the human-chimpanzee divergence.     

Globin-coupled sensors, protoglobins, and the last universal common ancestor

The strategy for detecting oxygen, carbon monoxide, nitric oxide, and sulfides is predominantly through heme-based sensors utilizing either a globin domain or a PAS domain. Whereas PAS domains bind various cofactors, globins bind only heme. Globin-coupled sensors (GCSs) were first described as regulators of the aerotactic responses in Bacillus subtilis and Halobacterium salinarum. GCSs were also identified in diverse microorganisms that appear to have roles in regulating gene expression. Functional and evolutionary analyses of the GCSs, their protoglobin ancestor, and their relationship to the last universal common ancestor (LUCA) are discussed in the context of globin-based signal transduction.     

A HERV-K provirus in chimpanzees, bonobos and gorillas, but not humans

Evidence from DNA sequencing studies strongly indicated that humans and chimpanzees are more closely related to each other than either is to gorillas [1-4]. However, precise details of the nature of the evolutionary separation of the lineage leading to humans from those leading to the African great apes have remained uncertain. The unique insertion sites of endogenous retroviruses, like those of other transposable genetic elements, should be useful for resolving phylogenetic relationships among closely related species. We identified a human endogenous retrovirus K (HERV-K) provirus that is present at the orthologous position in the gorilla and chimpanzee genomes, but not in the human genome. Humans contain an intact preintegration site at this locus. These observations provide very strong evidence that, for some fraction of the genome, chimpanzees, bonobos, and gorillas are more closely related to each other than they are to humans. They also show that HERV-K replicated as a virus and reinfected the germline of the common ancestor of the four modern species during the period of time when the lineages were separating and demonstrate the utility of using HERV-K to trace human evolution.     

Comparative genomics, minimal gene-sets and the last universal common ancestor

Comparative genomics, using computational and experimental methods, enables the identification of a minimal set of genes that is necessary and sufficient for sustaining a functional cell. For most essential cellular functions, two or more unrelated or distantly related proteins have evolved; only about 60 proteins, primarily those involved in translation, are common to all cellular life. The reconstruction of ancestral life-forms is based on the principle of evolutionary parsimony, but the size and composition of the reconstructed ancestral gene-repertoires depend on relative rates of gene loss and horizontal gene-transfer. The present estimate suggests a simple last universal common ancestor with only 500-600 genes.     

CvP-bias as an index to predict the life style of last common ancestor

CvP-bias (difference between proportions of charged and polar non-charged amino acids) has been recognized as an efficient criterion to distinguish hyperthermophiles from mesothermophiles. By analyzing the CvP-biases of seven barophiles's proteomes, we reveal that this criterion still works for barophiles. As a result, CvP-bias criterion is applicable to disclosing some secrets in the lifestyles of the last common ancestor (LCA), no matter the LCA lived in deep sea or not, which is helpful to building a self-consistent model for the LCA.     

Molecular paleontology and complexity in the last eukaryotic common ancestor

Abstract

Eukaryogenesis, the origin of the eukaryotic cell, represents one of the fundamental evolutionary transitions in the history of life on earth. This event, which is estimated to have occurred over one billion years ago, remains rather poorly understood. While some well-validated examples of fossil microbial eukaryotes for this time frame have been described, these can provide only basic morphology and the molecular machinery present in these organisms has remained unknown. Complete and partial genomic information has begun to fill this gap, and is being used to trace proteins and cellular traits to their roots and to provide unprecedented levels of resolution of structures, metabolic pathways and capabilities of organisms at these earliest points within the eukaryotic lineage. This is essentially allowing a molecular paleontology. What has emerged from these studies is spectacular cellular complexity prior to expansion of the eukaryotic lineages. Multiple reconstructed cellular systems indicate a very sophisticated biology, which by implication arose following the initial eukaryogenesis event but prior to eukaryotic radiation and provides a challenge in terms of explaining how these early eukaryotes arose and in understanding how they lived. Here, we provide brief overviews of several cellular systems and the major emerging conclusions, together with predictions for subsequent directions in evolution leading to extant taxa. We also consider what these reconstructions suggest about the life styles and capabilities of these earliest eukaryotes and the period of evolution between the radiation of eukaryotes and the eukaryogenesis event itself.     

Age of the last common ancestor of extant Plasmodium parasite lineages

Parasites of the genus Plasmodium infect all classes of amniotes (mammals, birds and reptiles) and display host specificity in their infections. It is therefore generally believed that Plasmodium parasites co-evolved intimately with their hosts. Here, we report that based on an evolutionary analysis using 22 genes in the nuclear genome, extant lineages of Plasmodium parasites originated roughly in the Oligocene epoch after the emergence of their hosts. This timing on the age of the common ancestor of extant Plasmodium parasites suggest the importance of host switches and lends support to the evolutionary scenario of a "malaria big bang" that was proposed based on the evolutionary analysis using the mitochondrial genome.     

About the last common ancestor, the universal life-tree and lateral gene transfer: a reappraisal

An organismal tree rooted in the bacterial branch and derived from a hyperthermophilic last common ancestor (LCA) is still widely assumed to represent the path followed by evolution from the most primeval cells to the three domains recognized among contemporary organisms: Bacteria, Archaea and Eucarya. In the past few years, however, more and more discrepancies between this pattern and individual protein trees have been brought to light. There has been an overall tendency to attribute these incongruities to widespread lateral gene transfer. However, recent developments, a reappraisal of earlier evidence and considerations of our own lead us to a quite different view. It would appear (i) that the role of lateral gene transfer was overemphasized in recent discussions of molecular phylogenies; (ii) that the LCA was probably a non-thermophilic protoeukaryote from which both Archaea and Bacteria emerged by reductive evolution but not as sister groups, in keeping with a current evolutionary scheme for the biosynthesis of membrane lipids; and (iii) that thermophilic Archaea may have been the first branch to diverge from the ancestral line.     

Age determination by immunological techniques of the last common ancestor of man and chimpanzee

Summary Following on from earlier work in this laboratory the age of the last common ancestor (LCA) of man and chimpanzee was determined by an immunogenetic approach. The determinant patterns of 30 different plasma-protein entities were examined for homologues in human and chimpanzee blood. Comparison of these determinants revealed the number of immunologically relevant accepted mutations separating the two species.The proteins investigated in this way were then employed as representatives of their corresponding structural genes, since their polypeptide sequences are direct translations of the latter, i.e. actually two samples of the genomes in question were compared.The subsequent calculation of the ages of the LCAs made use of previously estimated values for other primate groups including gorilla, orang utan, several Old World monkeys, one New World monkey and one prosimian. We used the same algorithm as in the earlier investigation for the present analysis.The result indicates that man and chimpanzee shared a common ancestor 9.7 million years ago. This value is lower than those determined for any other species investigated in our laboratory, including gorilla and orang utan. This reaffirms the special position of the chimpanzee among other primates in relation to man, which is otherwise expressed in anatomical, physiological and psychological features. The value given is dependent on the reference point employed to introduce absolute units. The age of the eutherian common ancestor, assumed to be 70 million years, was used for the present study. Relative time scales, dividing the same time interval into 100 relative time units, are better suited to describe the results, but do not allow any comparison with morphologically derived data.The method employed and the implications of the results obtained are discussed in some detail.

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Zusammenfassung In Fortführung früherer Untersuchungen unseres Arbeitskreises wurde das Alter des letzten gemeinsamen Vorfahren (LGV) des Menschen und des Schimpansen mit einer immungenetischen Technik bestimmt. Die Determinantenstrukturen von 30 Plasmaproteinen wurden jeweils für die Homologen der beiden Arten analysiert. Aus ihrem Vergleich ergibt sich die Zahl der immunologisch relevanten, akzeptierten Mutationen, in denen sich die beiden Species unterscheiden.Da die Polypeptidanteile der Proteine, welche die Determinanten tragen, direkte Übersetzungen der zugehörigen Strukturgene darstellen, ist die beschriebene Untersuchung zugleich eine solche einer Stichprobe der betreffenden Genome.Für die Berechnung des Alters des LGV von Mensch und Schimpanse wurden unsere früher erhaltenen Resultate für andere Primatengruppen zum Vergleich herangezogen. Diese umfaßten Gorilla und Orang Utan, einige Altweltaffen und je einen Neuwelt- und Halbaffen. Wir verwandten den gleichen Algorithmus wie früher beschrieben.Das so erhaltene Alter für den LGV von Mensch und Schimpanse beträgt 9,7 Millionen Jahre und ist damit kleiner als für jeden anderen bisher von uns untersuchten LGV des Menschen mit einer anderen Art; der Wert ist auch kleiner als für die Paare Mensch/Gorilla und Mensch/Orang Utan. Dieses Ergebnis bestätigt die besondere Stellung des Schimpansen unter allen Primaten zum Menschen, wie sie aus anatomischen, physiologischen und psychologischen Befunden erschlossen wurde. Zugleich werden die Möglichkeiten, welche die immungenetische Analyse in der Primatologie und Anthropologie eröffnet, erneut bestätigt.

     

Investigation of the RH locus in gorillas and chimpanzees

The human Rh blood-group system is encoded by two homologous genes,RhD andRhCE. TheRH genes in gorillas and chimpanzees were investigated to delineate the phylogeny of the humanRH genes. Southern blot analysis with an exon 7-specific probe suggested that gorillas have more than twoRH genes, as has recently been reported for chimpanzees. Exon 7 was well conserved between humans, gorillas, and chimpanzees, although the exon 7 nucleotide sequences from gorillas were more similar to the humanD gene, whereas the nucleotide sequences of this exon in chimpanzees were more similar to the humanCE gene. The intron between exon 4 and exon 5 is polymorphic and can be used to distinguish the humanD gene from theCE gene. Nucleotide sequencing revealed that the basis for the intron polymorphism is anAlu element inCE which is not present in theD gene. Examination of gorilla and chimpanzee genomic DNA for this intron polymorphism demonstrated that theD intron was present in all the chimpanzees and in all but one gorilla. TheCE intron was found in three of six gorillas, but in none of the seven chimpanzees. Sequence data suggested that theAlu element might have previously been present in the chimpanzeeRH genes but was eliminated by excision or recombination. Conservation of theRhD gene was also apparent from the complete identity between the 3′-noncoding region of the human D cDNA and a gorilla genomic clone, including anAlu element which is present in both species. The data suggest that at least twoRH genes were present in a common ancestor of humans, chimpanzees, and gorillas, and that additionalRH gene duplication has taken place in gorillas and chimpanzees. TheRhCE gene appears to have diverged more thanRhD among primates. In addition, theRhD gene deletion associated with the Rh-negative phenotype in humans seems to have occurred after speciation. Correspondence to: C.M. Westhoff     

Comparison of the communicative vocalizations and behaviors of group ranging in eastern gorillas,chimpanzees and pygmy chimpanzees

Field observations were carried out on chimpanzees, pygmy chimpanzees and eastern gorillas. Since the communicative behaviors which appear in group ranging are closely related to the grouping of the animals and to the social structure, the communicative behaviors of group ranging were compared in the above three species in order to elucidate the common and different characters of their three much diversified social structures. The following conclusions were drawn: (1) the common ancestor ofGorilla andPan had the territorial call “hoot” and behavior of display, and males were antagonistic between each other in the society; (2) the common ancestral species did not have any special long distance cohesive calling: the society was a small compact one, moving on the ground; and (3) the social structure of the pygmy chimpanzee is very different from the common ancestral social structure when compared with those of the gorilla and chimpanzee, in that the pygmy chimpanzee has lost the behaviors of strong antagonistic character between adult males.     

The genetic signature of sex-biased migration in patrilocal chimpanzees and humans

A large body of theoretical work suggests that analyses of variation at the maternally inherited mitochondrial (mt)DNA and the paternally inherited non-recombining portion of the Y chromosome (NRY) are a potentially powerful way to reveal the differing migratory histories of men and women across human societies. However, the few empirical studies comparing mtDNA and NRY variation and known patterns of sex-biased migration have produced conflicting results. Here we review some methodological reasons for these inconsistencies, and take them into account to provide an unbiased characterization of mtDNA and NRY variation in chimpanzees, one of the few mammalian taxa where males routinely remain in and females typically disperse from their natal groups. We show that patterns of mtDNA and NRY variation are more strongly contrasting in patrilocal chimpanzees compared with patrilocal human societies. The chimpanzee data we present here thus provide a valuable comparative benchmark of the patterns of mtDNA and NRY variation to be expected in a society with extremely female-biased dispersal.