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1 2m

Fig. 2. Inferred ancestral mammalian and ancestral primate karyotypes with the assignment of human homologies to the left, based on multidirectional chromosome painting data. The primate karyotype is derived by fissions of 10p and 12pter-q23.3, 16q and 19q, and 4 and 8p, followed by fusion of 10p/10q.

ancestral chromosome forms (7p21-q11.21, 7q11.23-21.3, 7q22.1-qter) and (7pter-p22, 7q11.21-n.23, 7q21.3-22.1)/16p. Human chromosomes 12 and 22 resulted from a reciprocal translocation t(12;22)(q23.3;q12.3) of the two ancestral homologs 10p/12pter-q23.3/22q12.3-qter and 22q11.2-22q12.3/12q23.3-qter. Chromosome 16q and 19q homologs are associated on a single chromosome, whereas 8q, 10q and 19p are found as separate entities (13) (Fig. 2). The ancestral karyotype of placental mammals may therefore have comprised of 2n=46 chromosomes.

The putative ancestral primate karyotype shows only a very few differences when compared to the ancestral mammalian karyotype. In the inferred primate ancestor presumably fissions of 10p and 12pter-q23.3, 16q and 19q, and 4 and 8p occurred, followed by fusion of 10p/10q, resulting in a karyotype of 2n = 50 chromosomes with conserved human homologous chromosome (segments) 1, 2pter-q13, 2q13-qter, 4, 5, 6, (7p21-q11.21, 7q11.23-21.3, 7q22.1-qter), 8p, 8q, 9, 10, 11, 13, 16q, 17, 18, 19p, 19q, 20, X, Y, and the association of 3/21, (7pter-p22, 7q11.21-11.23,7q21.3-22.1)/16p, 12pter-q23.3/22q12.3-qter, 22q11.2-22q12.3/12q23.3-qter, 14/15 (Fig. 2).

The following section provides an overview of the current knowledge on karyotype evolution in prosimians and higher primates (anthropoidea), the latter being subdivided in New World monkeys (platyrrhini), Old World monkeys (cercopithecoidea), and apes (hominoidea, gibbons, and great apes).

Prosimians

Prosimians are comprised of lorises, bush-babies, and lemurs. Only five species were fully analyzed using human chromosome painting probes: brown, black, and ring-tailed lemur (4,9), and two bush-babies (14). In addition, black lemur chromosome-specific probes were characterized by reverse painting to human chromosomes (4). The results so far revealed that these prosimians retained ancestral primate chromosome forms 12/22, 3/21, 14/15, and probably

7/16, but showed common derived fissions of chromosome 1 (two fissions), 4, 5, 6, 8, and 15. In addition, the investigated lemurs share four derived fissions and five translocations, the two bush-babies five fissions, and six translocations (14). Numerous further rearrangements were noticed, for example eight fusions only found in the black lemur (4). By conclusion, none of the prosimians analyzed to date has conserved a primitive primate karyotype, instead prosimians have highly derived karyotypes.

New World Monkeys

The 16 genera and over 100 recognized species of New World monkeys (platyrrhini) show a high degree of karyotypic diversity with chromosome numbers ranging from 2n = 16 in Callicebus lugens to 2n = 62 in Lagothrix lagotricha. With established comparative genome maps between human and more than 20 species by cross-species chromosome painting with human probes, New World monkeys represent the most comprehensively studied group of species among mammals altogether. In addition, several species have been analyzed by multidirectional chromosome painting employing tamarin (Saguinus oedipus) (15) and woolly monkey (L. lagothricha) (16) chromosome-specific probes.

In the inferred ancestral New World monkey karyotype of 2n = 54 chromosomes (17), human chromosomes 4, 6, 9, 11, 12, 13, 17, 19, 20, 22, X, and Y homologs are found entirely conserved as separate chromosomes. Chromosome 5, 14, 18, and 21 homologs show conserved synteny, are however associated with other homologs (5/7a, 14/15a, 8a/18, and 3a/21). The remaining human homologs are fragmented: 1a, 1b, 1c, 2a, 2b/16b, 3b, 3c, 7b, 8b, 10a/16a, 10b, and 15b.

Among the family callitrichidae, two tamarins (S. oedipus and Leontopithecus chrysomelas), three marmoset species (Callithrix jacchus, Cebuellapygmaea, and Callithrix argentata), and Callimico goeldii were analyzed by multidirectional chromosome painting (17-19). The data showed that C. goeldii exclusively shares derived syntenic associations 13/9/22 and 13/17/20 with all callithrichids. A study on an interspecies hybrid between a female Common marmoset (C. jacchus, 2n = 46) and a male Pygmy marmoset (C. pygmaea, 2n = 44) with a diploid chromosome number of 2n=45 gave further support for the inclusion of Cebuella within genus Callithrix (20). Genomic imbalances between this interspecies hybrid and other callithrichidae, visualized by interspecies Comparative genomic hybridization (iCGH), were confined to centromeric and subtelomeric heterochromatin. Cross-species FISH with a micro-dissection derived C. pygmaea repetitive probe revealed species-specificity of several 50 Mb and larger blocks of heterochromatin, thus providing a dramatic example for amplification of noncentromeric repetitive sequences within approximately 5 million years of evolution (20).

Zoo-FISH data are also available from the squirrel monkey, capucin monkeys, and three species of titi monkey (family cebidae). The squirrel monkey shares the derived syntenic association 2/15 with callithrichidae (17). Capuchin monkeys have conserved almost completely the ancestral New World monkey karyotype (21-23). Titi monkeys Callicebus moloch, Callicebus donacophilus (both 2n = 50), and C. lugens (2n = 16), are phylogenetically linked by common derived associations 10/11, 22/2/22, and 15/7 (24-26). The low chromosome number of C. lugens is the result of at least 22 fusions and 6 fissions.

The diploid chromosome numbers of atelidae (Howler monkeys, genus Alouatta, Spider monkeys, genusAteles, Wooly monkeys, genus Lagothrix, and Wooly spider monkeys, genus Brachyteles) range from 2n = 32 in Ateles to 2n=62 in Brachyteles and Lagothrix. Species from all four genera have been analyzed by multi-directional chromosome painting (16,27,28). All atelidae analyzed share the derived fissions of human chromosome 1, 4, and 5 homologs, inversion of the 10/16 and 5/7 homologs, and a translocation 4/15. The ancestral atelidae karyotype is comprised of 2n=62 chromosomes and is conserved in Lagothrix and Brachyteles. Howler monkeys represent the genus with the most extensive karyotype diversity within platyrrhini with high levels of intra-specific chromosomal variability (29,30,27). Molecular cytogenetic studies in Spider monkeys (genus Ateles) revealed that at least 17 fusions and three fissions are necessary to derive the putative ancestral Ateles karyotype conserved in A. b. marginatus (2n = 34) (23,28,31).

Old World Monkeys

Macaques and baboons have strongly conserved and uniform karyotypes with 2n = 42 chromosomes. Compared to the human karyotype all chromosomes show conserved synteny, except for two human chromosome 2 (two homologs) (32). The reduced chromosome number is the result of two fusions, leading to syntenic association of chromosome 7/21 and 20/22 homologs. They further conserved the primate ancestral association of14/15 homologs. Among guenons, fissions are the main mechanism driving the evolutionary trend toward higher chromosome numbers of 2n = 60 in the African green monkey (Chlorocebus aethiops) (33) and to 2n = 72 in Cercopithecus wolfi.

Leaf-eating monkeys have fairly conserved karyotypes, compared with human with chromosome numbers of 2n = 44 in the black and white colobus (Colobus guereza) (34) and 2n = 48 in the proboscis monkey (Nasalis larvatus) (35). These Colobines share the derived association of human chromosomes 21/22. The Asian members further share a reciprocal translocation of the human chromosome 1 and 19 homolog that was followed by a pericentric inversion.

Hominoids

The four gibbon subgenera show distinct karyomorphs with 2n = 38 in Bunopithecus, 2n = 44 in Hylobates, 2n = 50 in Symphalangus, and 2n = 52 in Nomascus. During the last decade all four subgenera were studied by Zoo-FISH, which revealed extensive chromosome reshuffling in all gibbons. First studies employed human chromosome paint probes (36-39). More recently, gibbons were reanalyzed by multidirectional painting (40-42).

The inferred ancestral karyotype of all extant gibbons differed from the putative ancestral hominoid karyotype by at least five reciprocal translocations, eight inversions, 10 fissions, and one fusion (42). It included homologs to human chromosomes 7, 9, 13, 14, 15, 20, 21, 22, X, and Y with conserved synteny and homologous segments of human chromosome 1 (three segments), 2, 3, 4, 5, 6 (two segments each), 8, 11, 12, and 17, respectively. Finally, syntenic associations of segments homologous to human chromosomes were included: 3/8, 3/12/19, 5/16, 5/16/5/16, 19/12/19, 10/4 (twice), 12/3/8, 17/2/17/2, and 18/11. The White-cheeked gibbon, Siamang and White-handed gibbon further share at least five common derived chromosome forms: associations 2/7, 8/3/11/18, 4/5, 22/5/16, and an inversion. In the last common ancestor of the White-cheeked gibbon and the Siamang, one fusion and four fissions may have occurred. In addition, each gibbon accumulated a large number of species-specific rearrangements (between 10 in the White-handed gibbon and 28 in the Hoolock).

Comparative high resolution G-banding analysis of human and great apes indicated, that the only interchromosomal changes are species-specific: a fusion of chromosome 2 in the human lineage, a reciprocal translocation t(5;17) in the gorilla and a band insertion ins(8;20) in the orangutan (44). Chromosome painting of great ape genomes with human probes confirmed the

Fig. 3. Superimposition of primate evolutionary landmark rearrangements onto the consensus phylogenetic tree.

fusion of human chromosome 2 and the translocation t(5;17) in the gorilla, but not the insertion ins(8;20) in the orangutan (1,36,43). Further, G-banding indicated that human and great ape genomes would differ by the presence and chromosomal location of constitutive heterochro-matin, in the number of nucleolar organizer region-bearing chromosomes, and by several inversions (44). For example, chimpanzee and human chromosome 1, 4, 5, 9, 12, 15, 16, 17, and 18 homologs would differ by pericentric inversions and chromosome 7 homologs of chimpanzee and gorilla by a paracentric inversion. Human and gorilla chromosome 16 homologs as well as human and orangutan chromosome 3 and 17 homologs would have diverged by both peri- and paracentric inversions.

Primate Evolutionary Landmark Rearrangements

On the basis of molecular cytogenetic evidence it is possible to draw increasingly accurate conclusions on landmark rearrangements that occurred during primate evolution (Fig. 3). These landmarks are shared by defined subgroups of primates and thus provide fundamental phylogenetic links between members of these species groups. They can further be superimposed onto the consensus primate phylogenetic tree, which permits an estimate of the timing of these events. The putative ancestor of all primates most probably acquired separate chromosomes 4 and 10 homologs by fission/fusion events and lost the association of16/19 homologs by fission about 60 million years ago (Fig. 2). The inferred ancestor of higher primates only retained ancestral primate syntenic associations 14/15 and 3/21, but acquired separate chromosome 12 and 22 homologs by reciprocal translocation, a single chromosome 19 homolog by

Fig. 4. Overview on chromosome rearrangements that occurred in orangutan, gorilla, chimpanzee and human (see The Evolutionary History of Human Chromosomes for details).

a fusion, and lost the association of human 7/16 homologs by fission. These events can be dated before the emergence of New and Old World monkeys (approx 30-40 million years ago). After the New/Old World monkey split, platyrrhini acquired common derived associations 5/7, 2/16, 10/16, 8/18, and several fissions, whereas in the catarrhini ancestor (about 25 million years ago) a fission led to separate chromosomes 3 and 21, whereas fusions resulted in single chromosome 7, 8, and 16 homologs. Approximately 18 million years ago, in the common ancestor of hominoids fission of the association 14/15 took place, leading to separate chromosomes 14 and 15. Finally, less than 6 million years ago and after the divergence of human and chimpanzee, the fusion of human chromosome 2 occurred (Fig. 3).

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