Chromosomal Rearrangements in the Human and Chimpanzee Lineages

Hildegard Kehrer‐Sawatzki, University of Ulm, Ulm, Germany
David N Cooper, Cardiff University, Cardiff, UK

Published online: May 2008

DOI: 10.1002/9780470015902.a0020738

Among the structural differences evident between humans and chimpanzees are large chromosomal rearrangements which are visible by cytogenetic analysis. These include the fusion that created human chromosome 2, nine pericentric inversions and numerous chromatin additions at the telomeres. Recently performed genome-wide comparative analyses have also revealed a considerable number of submicroscopic structural variations which contribute significantly to the chromosomal divergence between humans and chimpanzees. This microheterogeneity comprises inversions, duplications and deletions ranging in size from a few base pairs up to several megabases. These copy number differences appear to have given rise to several hundred megabases of genomic deoxyribonucleic acid (DNA) sequence that are either present or absent in humans as compared to chimpanzees. Since many of these lineage-specific copy number differences contain genes, humans and chimpanzees may differ significantly with respect to their gene content, and some of these differences could have influenced the evolution of lineage-specific traits.

Keywords: pericentric inversions; fusion of human chromosome 2; suppressed recombination; microheterogeneity; copy number differences; microinversions

Figure 1. G-banded chromosomes of human (upper panel) and chimpanzee chromosomes (Pan troglodytes, lower panel). Human chromosome 2 and the two submetacentric orthologous chimpanzee chromosomes are boxed by grey rectangles. The positions of the centromeres of these submetacentric chromosomes are indicated by black lines. The two ancestral chromosomes to these chimpanzee chromosomes gave rise to human chromosome 2 by telomere–telomere fusion. The human and chimpanzee chromosomes that are distinguishable by pericentric inversions are indicated by red and green arrowheads, respectively.
Figure 2. Model to explain the probable mechanism underlying the human-specific inversion of chromosome 18. This inversion was probably mediated by a human lineage-specific segmental duplication (grey striped arrow) in inverted orientation that was transposed to the p arm in the ancestor of modern humans (cen: centromere).
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 References
    Ayala FJ and Coluzzi M (2005) Chromosome speciation: humans, Drosophila, and mosquitoes. Proceedings of the National Academy of Sciences of the USA 102: 6535–6542.
    Cheng Z, Ventura M, She X et al. (2005) A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437: 88–93.
    Demuth JP, Bie TD, Stajich JE, Cristianini N and Hahn MW (2006) The evolution of mammalian gene families. PLoS ONE 1: e85.
    Fan Y, Linardopoulou E, Friedman C, Williams E and Trask BJ (2002) Genomic structure and evolution of the ancestral chromosome fusion site in 2q13–2q14.1 and paralogous regions on other human chromosomes. Genome Research 12: 1651–1662.
    Feuk L, Macdonald JR, Tang T et al. (2005) Discovery of human inversion polymorphisms by comparative analysis of human and chimpanzee DNA sequence assemblies. PLoS Genetics 1: e56.
    Fortna A, Kim Y, MacLaren E et al. (2004) Lineage-specific gene duplication and loss in human and great ape evolution. PLoS Biology 2: e207.
    Hughes JF, Skaletsky H, Pyntikova T et al. (2005) Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee. Nature 437: 100–103.
    Kehrer-Sawatzki H and Cooper DN (2007) Structural divergence between the human and chimpanzee genomes. Human Genetics 120: 759–778.
    Kehrer-Sawatzki H, Sandig C, Chuzhanova N et al. (2005) Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes). Human Mutation 25: 45–55.
    Kuroki Y, Toyoda A, Noguchi H et al. (2006) Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nature Genetics 38: 158–167.
    Linardopoulou EV, Williams EM, Fan Y et al. (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94–100.
    Lu J, Li WH and Wu CI (2003) Comment on “Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes”. Science 302: 988.
    Navarro A and Barton NH (2003) Chromosomal speciation and molecular divergence – accelerated evolution in rearranged chromosomes. Science 300: 321–324.
    Newman TL, Tuzun E, Morrison VA et al. (2005) A genome-wide survey of structural variation between human and chimpanzee. Genome Research 15: 1344–1356.
    Noor MA, Grams KL, Bertucci LA and Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the USA 98: 12084–12088.
    Page DC, Harper ME, Love J and Botstein D (1984) Occurrence of a transposition from the X-chromosome long arm to the Y-chromosome short arm during human evolution. Nature 311: 119–123.
    Patterson N, Richter DJ, Gnerre S, Lander ES and Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441: 1103–1108.
    Popesco MC, Maclaren EJ, Hopkins J et al. (2006) Human lineage-specific amplification, selection, and neuronal expression of DUF1220 domains. Science 313: 1304–1307.
    Ranz JM, Maurin D, Chan YS et al. (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biology 5(6): e152.
    Rhesus Macaque Genome Sequencing and Analysis Consortium, Gibbs RA, Rogers J et al. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222–234.
    Skaletsky H, Kuroda-Kawaguchi T, Minx PJ et al. (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825–837.
    Szamalek JM, Cooper DN, Hoegel J, Hameister H and Kehrer-Sawatzki H (2007) Chromosomal speciation of humans and chimpanzees revisited: studies of DNA divergence within inverted regions. Cytogenetic and Genome Research 116: 53–60.
    Szamalek JM, Cooper DN, Schempp W et al. (2006b) Polymorphic micro-inversions contribute to the genomic variability of humans and chimpanzees. Human Genetics 119: 103–112.
    Szamalek JM, Goidts V, Chuzhanova N et al. (2005) Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Human Genetics 117: 168–176.
    Szamalek JM, Goidts V, Searle JB et al. (2006a) The chimpanzee-specific pericentric inversions that distinguish humans and chimpanzees have identical breakpoints in Pan troglodytes and Pan paniscus. Genomics 87: 39–45.
    Vallender EJ and Lahn BT (2004) Effects of chromosomal rearrangements on human–chimpanzee molecular evolution. Genomics 84: 757–761.
    Won YJ and Hey J (2005) Divergence population genetics of chimpanzees. Molecular Biology and Evolution 22: 297–307.
    Yoder AD and Yang Z (2000) Estimation of primate speciation dates using local molecular clocks. Molecular Biology and Evolution 17: 1081–1090.
    Yunis JJ and Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215: 1525–1530.
    Zhang J, Wang X and Podlaha O (2004) Testing the chromosomal speciation hypothesis for humans and chimpanzees. Genome Research 14: 845–851.
 Further Reading
    Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69–87.
    Dennehey BK, Gutches DG, McConkey EH and Krauter KS (2004) Inversion, duplication, and changes in gene context are associated with human chromosome 18 evolution. Genomics 83: 493–501.
    van Geel M, Eichler EE, Beck AF et al. (2002) A cascade of complex subtelomeric duplications during the evolution of the hominoid and Old World monkey genomes. American Journal of Human Genetics 70: 269–278.
    Kehrer-Sawatzki H, Sandig CA, Goidts V and Hameister H (2005) Breakpoint analysis of the pericentric inversion between chimpanzee chromosome 10 and the homologous chromosome 12 in humans. Cytogenetic and Genome Research 108: 91–97.
    Noonan JP, Coop G, Kudaravalli S et al. (2006) Sequencing and analysis of Neanderthal genomic DNA. Science 314: 1113–1118.
    Rieseberg LH and Livingstone K (2003) Evolution. Chromosomal speciation in primates. Science 300: 267–268.
    Wienberg J (2005) Fluorescence in situ hybridization to chromosomes as a tool to understand human and primate genome evolution. Cytogenetic and Genome Research 108: 139–160.
    Wilson GM, Flibotte S, Missirlis PI et al. (2006) Identification by full-coverage array CGH of human DNA copy number increases relative to chimpanzee and gorilla. Genome Research 16: 173–181.

Related Sub-Topics:

Evolutionary Genomics | Molecular Evolution | Human Evolution | Chromosomes and Chromatin Modifications | Evolution of Coding and Functional Modules
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Article Title: Chromosomal Rearrangements in the Human and Chimpanzee Lineages
 
How to Cite close
Kehrer‐Sawatzki, Hildegard, and Cooper, David N(May 2008) Chromosomal Rearrangements in the Human and Chimpanzee Lineages. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020738]