Conservation of human-derived pseudoautosomal sequences on the sex chromosomes of the great apes

In situ hybridization using a repeated element specific for the human pseudoautosomal region, DXYZ2, revealed the presence of this repeat in the early replicating portion of the sex chromosomes of the great apes. This segment, as well as the DXYZ2 repeats, are located in band Xp22.3 and in a telomeric or subtelomeric region of the Y chromosome. These segments may therefore represent pseudoautosomal regions, as in man.     

Fluorescent (F) bodies in the spermatozoa of man and the great apes

Mature spermatozoa of the chimpanzee (Pan troglodytes), the gorilla (Gorilla gorilla), and the orangutan (Pongo pygmaeus) were stained with quinacrine dihydrochloride. Fluorescent (F) bodies were visualized in the spermatozoa of the chimpanzee and gorilla but were absent in the orangutan, in which there is no brilliant fluorescence in any chromosome. The F bodies appeared to be randomly located in the sperm heads of these two species, as they usually are in human spermatozoa. However, the proportion of sperm showing one or more F bodies in the chimpanzee and gorilla was not comparable to what is usually found in man. The F bodies in the chimpanzee presumably represent brilliant regions in the autosomes, since the Y chromosome has no brilliant fluorescence in this species. This is contrary to man, in which the F body is an useful indicator of the Y chromosome. In the gorilla, the F bodies probably correspond to both the Y chromosome and to some brilliant regions in the autosomes.     

Chromosome phylogenies of man,great apes,and old world monkeys

The karyotypes of man and of the closely related Pongidae — chimpanzee, gorilla, and orangutan — differ by a small number of well known rearrangements, mainly pericentric inversions and one fusion which reduced the chromosome number from 48 in the Pongidae to 46 in man. Dutrillaux et al. (1973, 1975, 1979) reconstructed the chromosomal phylogeny of the entire primate order. More and more distantly related species were compared thus moving backward in evolution to the common ancestors of the Pongidae, of the Cercopithecoidae, the Catarrhini, the Platyrrhini, the Prosimians, and finally the common ancestor of all primates. Descending the pyramid it becomes possible to assign the rearrangements that occurred in each phylum, and the one that led to man in particular.The main conclusions are that this phylogeny is compatible with the occurrence during evolution of simple chromosome rearrangements — inversions, fusions, reciprocal translocation, acquisition or loss of heterochromatin — and that it is entirely consistent with the known primate phylogeny based on physical morphology and molecular evolution. If heterochromatin is not taken into account, man has in common with the other primates practically all of his chromosomal material as determined by chromosome banding. However, it is arranged differently, according to species, on account of chromosome rearrangements. This interpretation has been confirmed by comparative gene mapping, which established that the same chromosome segments, identified by banding, carry the same genes (Finaz et al., 1973; Human Gene Mapping 8, 1985).A remarkable observation made by Dutrillaux is that different primate phyla seem to have adopted different chromosome rearrangements in the course of evolution: inversions for the Pongidae, Robertsonian fusions for the lemurs, etc. This observation may raise many questions, among which is that of an organized evolution. Also, the breakpoints of chromosomal rearrangements observed during evolution, in human chromosomal diseases, and after ionizing irradiation do not seem to be distributed at random.Chromosomal rearrangements observed in evolution are known to be harmful in humans, leading to complete or partial sterility through abnormal offspring in the heterozygous state but not in the homozygous state. They then become a robust reproductive barrier capable of creating new species, far more powerful than gene mutations advocated by neo-Darwinism. The homozygous state may be achieved especially through inbreeding, which must have played a major role during primate evolution. Whether new species derive from unique individuals or couples (Adam and Eve), or through a populational process, remains a matter for discussion.     

Unique genomic sequences in human chromosome 16p are conserved in the great apes

In humans, acute myelomonocytic leukemia (AMML) with abnormal bone marrow eosinophilia is diagnosed by the presence of a pericentric inversion in chromosome 16, involving breakpoints p13;q23 [i.e., inv(16)(p13;q23)]. A pericentric inversion involves breaks that have occurred on the p and q arms and the segment in between is rotated 180° and reattaches. The recent development of a “human micro-coatasome” painting probe for 16p contains unique DNA sequences that fluorescently label only the short arm of chromosome 16, which facilitates the identification of such inversions and represents an ideal tool for analyzing the “divergence/convergence” of the equivalent human chromosome 16 (PTR 18, GGO 17 and PPY 19) in the great apes, chimpanzee, gorilla and orangutan. When the probe is used on the type of pericentric inversion characteristic of AMML, signals are observed on the proximal portions (the regions closest to the centromere) of the long and short arms of chromosome 16. The probe hybridized to only the short arm of all three ape chromosomes and signals were not observed on the long arms, suggesting that a pericentric inversion similar to that seen in AMML has not occurred in any of these great apes. Received: 4 July 1996 / Accepted: 18 September 1996     

Sequence of DNA replication in Macaca juscata chromosomes: An outgroup for phylogenetic comparison between man and apes

The relative replication times of every band in the standardized 300 band G-band idiogram of the chromosomes of the Japanese macaque are presented, and compared to the human sequence. Many chromosomes thought to be homologous between Macaca fuscata and man on the basis of standard chromosome banding and gene mapping show a conservation of the replication sequence. Other supposed chromosomal homologies between these two species show no good correspondence, and the replication sequence data suggest that these chromosomes have been subject to complex rearrangements. The replication sequence data also point to possible additional chromosomal homologies between man and M. fuscata. Asynchrony in replication time between homologues from the same cell may also be evolutionarily conserved, because these species share a number of asynchronous homologous bands. Replication band sequence data can provide significant information for comparative cytogenetics. However, usually only the full replication R- or G-band pattern has been used for interspecific comparisons. The dynamic sequence data presented here determine the replication time of every band in the karyotype, and provide a quantitatively and qualitatively more sensitive tool to characterize chromosomes. Such data could provide valuable new information on which to make phylogenetic reconstructions, and shed light on the relationship between chromosome change and evolutionary process. Finally, the M. fuscata replication sequence presented here will provide a necessary foundation for future comparisons between apes and man.     

Giemsa staining of the sites replicating DNA early in human lymphocyte chromosomes.

A timetable for the initiation of DNA replication in human lymphocyte chromosomes has been established by a technique which allows detection of areas of chromosomes replicating at a given interval of the S-phase. The resolution of the method, using 33258 Hoechst-Giemsa staining, is more refined than that obtained with 3H-thymidine autoradiography. Early replicating regions coincide with R-bands. The timetable is rather coarse since replication may start asynchronously in the same region of homologous autosomes of the same metaphase and since even the sequence of bands appearing on individual chromosomes sometimes deviates from the rule.     

Mother-infant separation and reunion in the great apes

One mother-infant dyad of each species of great ape, orang-utan, chimpanzee and gorilla, with an additional conspecific cagemate, were studied for the effects of maternal separation and reunion. High levels of agitation were observed in all infants immediately upon separation, followed by a longer period of behavioral depression with continuing, intermittent agitation. A compatible cagemate seemed to attenuate, to some degree, the behavioral depression reaction. Initial detachment following reunion with the mother occurred for all the great ape infants studied. Subsequent intensification of mother-infant attachment occurred during reunion for all three species. The findings of intermittent agitation during separation and the initial detachment upon reunion with the mother are not generally reported for monkeys, but are reported for human children. These data suggest that certain responses to maternal separation and reunion occur, to some degree, among all primates that have been studied, whereas other responses seen among apes and humans are not generally reported for monkeys.     

Mammalian sex-chromosome evolution: a conserved homoeologous segment on the X and Y chromosomes in primates

In a representative sample of primate species, including simians (Catarrhini and Platyrrhini) and prosimians (Lemuriformes and Lorisiformes), high-resolution, early replication banding revealed a homoeologous early replicating segment at the ends of both sex chromosomes. The DXYZ2 element, a repeated sequence specific for the human pseudoautosomal region, is conserved in the genomes of all primate species studies and is specifically localized in the distal early replicating segments of the X and Y chromosomes. Thus, cytogenetic and molecular evidence is presented of a highly conserved sex-chromosomal segment in primates. The pseudoautosomal behavior of this segment is discussed.     

A human moderately repeated Y-specific DNA sequence is evolutionarily conserved in the Y chromosome of the great apes.

Evolutionary conservation of the human-derived moderately repeated Y-specific DNA sequence Y-190 (DYZ5) was investigated in the chimpanzee, orangutan, and gorilla. Southern blot analysis showed the presence of the sequence in the Y chromosome of all great apes. Pulsed-field gel electrophoresis and in situ hybridization revealed that the repeat is organized in one major block and confined to a small region of the Y chromosome of the three species. DYZ5 was assigned to the proximal short arm of the Y chromosome of the chimpanzee and orangutan and to the long arm of the Y chromosome of the gorilla. In light of its evolutionary conservation, DYZ5 may have an as yet undetermined structural function in the Y chromosome.     

Ruminant diets and the Miocene extinction of European great apes

The successful evolutionary radiations of European hominoids and pliopithecoids came to an end during the Late Miocene. Using ruminant diets as environmental proxies, it becomes possible to detect variations in vegetation over time with the potential to explain fluctuations in primate diversity along a NW–SE European transect. Analysis shows that ruminants had diverse diets when primate diversity reached its peak, with more grazers in eastern Europe and more browsers farther west. After the drop in primate diversity, grazers accounted for a greater part of western and central European communities. Eastwards, the converse trend was evident with more browsing ruminants. These opposite trends indicate habitat loss and an increase in environmental uniformity that may have severely favoured the decline of primate diversity.     

Characterization of the human lineage-specific pericentric inversion that distinguishes human chromosome 1 from the homologous chromosomes of the great apes

The human and chimpanzee genomes are distinguishable in terms of ten gross karyotypic differences including nine pericentric inversions and a chromosomal fusion. Seven of these large pericentric inversions are chimpanzee-specific whereas two of them, involving human chromosomes 1 and 18, were fixed in the human lineage after the divergence of humans and chimpanzees. We have performed detailed molecular and computational characterization of the breakpoint regions of the human-specific inversion of chromosome 1. FISH analysis and sequence comparisons together revealed that the pericentromeric region of HSA 1 contains numerous segmental duplications that display a high degree of sequence similarity between both chromosomal arms. Detailed analysis of these regions has allowed us to refine the p-arm breakpoint region to a 154.2 kb interval at 1p11.2 and the q-arm breakpoint region to a 562.6 kb interval at 1q21.1. Both breakpoint regions contain human-specific segmental duplications arranged in inverted orientation. We therefore propose that the pericentric inversion of HSA 1 was mediated by intra-chromosomal non-homologous recombination between these highly homologous segmental duplications that had themselves arisen only recently in the human lineage by duplicative transposition.Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .Justyna M. Szamalek and Violaine Goidts are contributed equally to the paper.