Role of Chromosomal Reorganisations in the Human–Chimpanzee Speciation


The elucidation of how recombination is shaping the genomic architecture of organisms and, more in particular, how this affects the speciation process has been a long‐standing question in evolutionary biology. Large‐scale genomic changes such as inversions, translocations, fusions and fissions contribute to the reshuffling of genomes, providing new chromosomal forms on which natural selection can work. Despite large efforts employed in the last decade, few empirical data are available on the mechanisms by which genome reshuffling contribute to the formation of new species. Here, the authors discuss on the models of chromosomal evolution and the contribution of chromosomal reorganisations in mammalian chromosome evolution, and more specifically, during the human–chimpanzee speciation event.

Key Concepts:

  • The evolutionary process by which new biological species arise (speciation) is a complex process that requires the understanding of many mechanisms such as reproductive isolation, patterns of species diversity, together with the genetic basis underlying the process.

  • Understanding the mechanisms by which reproductive isolation (breakdown of gene flow between two populations) is achieved, is fundamental for speciation.

  • Genetic speciation makes references to the group of genes that are involved in maintaining reproductive isolation between species.

  • Chromosomal reorganisations may contribute to speciation due to the underdominant fitness effects associated with meiotic abnormalities when occurring in heterozygotes.

  • Chromosome rearrangements, such as inversions, can suppress recombination thus contributing to a reduction of gene flow across genomic regions and the accumulation of genetic incompatibilities.

Keywords: chromosomal reorganisations; speciation; inversions; fusions; recombination; great apes; human; chimpanzee

Figure 1.

Representation of the different types of balanced chromosomal reorganisations (fusion, fission, inversion and translocation) that can contribute to chromosome evolution. Chromosomal arms are colour coded, whereas yellow arrows and horizontal bars depict regions where double stand breaks occur along the chromosomes. The centromeres are shown as sloped bars.

Figure 2.

Evolutionary history of human chromosomes superimposed on the phylogeny of great apes. Phylogeny and divergence times are based on previous studies (Locke et al., ; Scally et al., ; Prado‐Martinez et al., ). For each speciation node, effective population size is indicated (Scally et al., ; Prado‐Martinez et al., ). Chromosome 7 has suffered one inversion, fixed in gorilla, and another inversion fixed in human–chimpanzee ancestor. Chromosome 10 underwent one inversion fixed in humans and chimpanzees, and a new inversion fixed in gorilla. Finally, chromosome 12 has maintained the ancestral form in humans and orangutans but has undergone an inversion that has been fixed in chimpanzee and gorilla; therefore, the polymorphic state has persisted across multiple speciation nodes (gorilla–human–chimpanzee and human–chimp).

Figure 3.

Distribution of recombination rates in human chromosome 4. Recombination rates (y‐axis) are shown as needles across nonoverlapping windows of 10 kb in the whole chromosomal length (x‐axis). The genomic region affected by an inversion is depicted in grey, whereas noninverted regions are showed in black. The white rectangle indicates the centromere. Average recombination rate for each region is shown in numbers in the x‐axis. Redrawn from Farré et al. (). © Oxford University Press.



Ashley T, Moses MJ and Solari AJ (1981) Fine structure and behaviour of a pericentric inversion in the sand rat, Psammomys obesus . Journal of Cell Science 50: 105–119.

Auton A, Fledel‐Alon A, Pfeifer S et al. (2012) A fine‐scale chimpanzee genetic map from population sequencing. Science 336: 193–198.

Besansky NJ, Krzywinski J, Lehmann T et al. (2003) Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proceedings of the National Academy of Sciences of the USA 100(19): 10818–10823.

Borodin PM, Karamysheva TV, Belonogova NM et al. (2008) Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia). Genetics 178(2): 621–632.

Butlin RK and Ritchie MG (2009) Genetics of speciation. Heredity 102(1): 1–3.

Castiglia R and Capanna E (2002) Chiasma repatterning across a chromosomal hybrid zone between chromosomal races of Mus musculus domesticus . Genetica 114(1): 35–40.

Chaisson MJ, Raphael BJ and Pevzner PA (2006) Microinversions in mammalian evolution. Proceedings of the National Academy of Sciences of the USA 103(52): 19824–19829.

Clark AG, Wang X and Matise T (2010) Contrasting methods of quantifying fine structure of human recombination. Annual Review of Genomics and Human Genetics 11: 45–64.

Dobzhansky T and Sturtevant AH (1938) Inversions in the chromosomes of Drosophila pseudoobscura . Genetics 23(1): 28–64.

Dumas D and Britton‐Davidian J (2002) Chromosomal rearrangements and evolution of recombination: comparison of chiasma distribution patterns in standard and robertsonian populations of the house mouse. Genetics 162(3): 1355–1366.

Dumont BL and Payseur BA (2011) Genetic analysis of genome‐scale recombination rate evolution in house mice. PLoS Genetics 7(6): e1002116.

Faria R and Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends in Ecology & Evolution 25(11): 660–669.

Farré M, Micheletti D and Ruiz‐Herrera A (2013) Recombination rates and genomic shuffling in human and chimpanzee – a new twist in the chromosomal speciation theory. Molecular Biology and Evolution 30(4): 853–864.

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(4): e56.

Franchini P, Colangelo P, Solano E et al. (2010) Reduced gene flow at pericentromeric loci in a hybrid zone involving chromosomal races of the house mouse Mus musculus domesticus. Evolution 64(7): 2020–2032.

Garcia‐Cruz R, Pacheco S, Brieno MA et al. (2011) A comparative study of the recombination pattern in three species of Platyrrhini monkeys (primates). Chromosoma 120(5): 521–530.

Greenbaum IF and Reed MJ (1984) Evidence for heterosynaptic pairing of the inverted segment in pericentric inversion heterozygotes of the deer mouse (Peromyscus maniculatus). Cytogenetics and Cell Genetics 38(2): 106–111.

Jacques P‐É, Jeyakani J and Bourque G (2013) The majority of primate‐specific regulatory sequences are derived from transposable elements. PLoS Genetics 9(5): e1003504.

Kehrer‐Sawatzki H and Cooper DN (2008) Molecular mechanisms of chromosomal rearrangement during primate evolution. Chromosome Research 16(1): 41–56.

Kirkpatrick M and Barton N (2006) Chromosome inversions, local adaptation and speciation. Genetics 173(1): 419–434.

Kohn M, Hogel J, Vogel W et al. (2006) Reconstruction of a 450‐My‐old ancestral vertebrate protokaryotype. Trends in Genetics 22(4): 203–210.

Kong A, Thorleifsson G, Gudbjartsson DF et al. (2010) Fine‐scale recombination rate differences between sexes, populations and individuals. Nature 467(7319): 1099–1103.

Kulathinal RJ, Bennett SM, Fitzpatrick CL and Noor MA (2008) Fine‐scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proceedings of the National Academy of Sciences of the USA 105(29): 10051–10056.

Locke DP, Hillier LW, Warren WC et al. (2011) Comparative and demographic analysis of orang‐utan genomes. Nature 469(7331): 529–533.

Lowe CB and Haussler D (2012) 29 Mammalian genomes reveal novel exaptations of mobile elements for likely regulatory functions in the human genome. PLoS One 7(8): e43128.

Lynn A, Ashley T and Hassold T (2004) Variation in human meiotic recombination. Annual Review of Genomics and Human Genetics 5: 317–349.

Lynn A, Koehler KE, Judis L et al. (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296(5576): 2222–2225.

Marie Curie SPECIATION Network, Butlin R, Debelle A et al. (2012) What do we need to know about speciation? Trends in Ecology and Evolution 27(1): 27–39. doi: 10.1016/j.tree.2011.09.002.

Marques‐Bonet T, Caceres M, Bertranpetit J et al. (2004) Chromosomal rearrangements and the genomic distribution of gene‐expression divergence in humans and chimpanzees. Trends in Genetics 20(11): 524–529.

Marques‐Bonet T, Sanchez‐Ruiz J, Armengol L et al. (2007) On the association between chromosomal rearrangements and genic evolution in humans and chimpanzees. Genome Biology 8(10): R230.

Meredith RW, Janecka JE, Gatesy J et al. (2011) Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055): 521–524.

Michel AP, Grushko O, Guelbeogo WM et al. (2006) Divergence with gene flow in Anopheles funestus from the Sudan Savanna of Burkina Faso, West Africa. Genetics 173(3): 1389–1395.

Muller S and Wienberg J (2001) “Bar‐coding” primate chromosomes: molecular cytogenetic screening for the ancestral hominoid karyotype. Human Genetics 109(1): 85–94.

Navarro A and Barton NH (2003) Chromosomal speciation and molecular divergence – accelerated evolution in rearranged chromosomes. Science 300(5617): 321–324.

Navarro A and Ruiz A (1997) On the fertility effects of pericentric inversions. Genetics 147(2): 931–933.

Noor MA and Bennett SM (2009) Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103(6): 439–444.

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(21): 12084–12088.

Paigen K and Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nature Reviews Genetics 11(3): 221–233.

Prado‐Martinez J, Sudmant PH, Kidd JM et al. (2013) Great ape genetic diversity and population history. Nature 499(7459): 471–475.

Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends in Ecology & Evolution 16(7): 351–358.

Rieseberg LH, Whitton J and Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152(2): 713–727.

Rieseberg LH and Willis JH (2007) Plant speciation. Science 317(5840): 910–914.

Ruiz‐Herrera A, Farre M and Robinson TJ (2012) Molecular cytogenetic and genomic insights into chromosomal evolution. Heredity 108(1): 28–36.

Scally A, Dutheil JY, Hillier LW et al. (2012) Insights into hominid evolution from the gorilla genome sequence. Nature 483(7388): 169–175.

Segura J, Ferretti L, Ramos‐Onsins S et al. (2013) Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proceedings. Biological Sciences/The Royal Society 280(1771): 20131945.

Smukowski CS and Noor MA (2011) Recombination rate variation in closely related species. Heredity 107(6): 496–508.

Sun F, Trpkov K, Rademaker A, Ko E and Martin RH (2005) Variation in meiotic recombination frequencies among human males. Human Genetics 116(3): 172–178.

Uno Y, Nishida C, Tarui H et al. (2012) Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS One 7(12): e53027.

Vallender EJ and Lahn BT (2004) Effects of chromosomal rearrangements on human–chimpanzee molecular evolution. Genomics 84(4): 757–761.

Voss SR, Kump DK, Putta S et al. (2011) Origin of amphibian and avian chromosomes by fission, fusion, and retention of ancestral chromosomes. Genome Research 21(8): 1306–1312.

White BJ, Crandall C, Raveche ES and Hjio JH (1978) Laboratory mice carrying three pairs of Robertsonian translocations: establishment of a strain and analysis of meiotic segregation. Cytogenetics and Cell Genetics 21(3): 113–138.

Wu ZK, Getun IV and Bois PR (2010) Anatomy of mouse recombination hot spots. Nucleic Acids Research 38(7): 2346–2354.

Yunis JJ and Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215(4539): 1525–1530.

Zhang J, Wang X and Podlaha O (2004) Testing the chromosomal speciation hypothesis for humans and chimpanzees. Genome Research 14(5): 845–851.

Further Reading

Abbott R, Albach D, Ansell S et al. (2012) Hybridization and speciation. Journal of Evolutionary Biology 26: 229–246.

Ayala FJ and Coluzzi M (2005) Chromosome speciation: humans, Drosophila, and mosquitoes. Proceedings of the National Academy of Sciences of the USA 102(Suppl 1): 6535–6542.

Nachman MW and Payseur BA (2012) Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 409–421.

Rieseberg LH and Livingstone K (2003) Chromosomal speciation in primates. Science 300: 267–268.

Stumpf MPH and Mcvean GAT (2003) Estimating recombination rates from population‐genetic data. Nature Reviews Genetics 4: 959–968.

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Farré, Marta, and Ruiz‐Herrera, Aurora(May 2014) Role of Chromosomal Reorganisations in the Human–Chimpanzee Speciation. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0025534]