Speciation: Chromosomal Mechanisms

Abstract

Chromosomal speciation is one of the major modes of the origin of new species through the splitting of preexisting species. New species may originate by gene speciation, and also by the establishment of post‐mating reproductive isolation through structural chromosome rearrangements. The latter may induce low‐hybrid fitness, generated by macromutations, and even by micromutations, that is, molecular changes causing meiotic disturbances (e.g. GC incompatibilities), although the latter awaits empirical support. Criticism against the traditional model of chromosomal speciation led to renewed theoretical models arguing that chromosomal rearrangements can generate reproductive isolation between species by suppressing recombination within rearranged regions. Reduced recombination permits the accumulation of alleles contributing to reproductive isolation and adaptive divergence and radiation. Likewise, coding and noncoding genomes, and novel chromosomal breakpoint regions can generate novel combinations of genes and regulatory elements that contribute to both adaptive radiation and ecological speciation. Chromosomal speciation is certainly an important speciation mode across life, although we cannot yet quantify it in relation to other modes. The spalacid example of blind subterranean mole rats in the East Mediterranean is presented as a widely studied case of chromosomal ecological speciation. The proportion of chromosomal speciation in nature, particularly in animals, remains a future challenge.

Key Concepts:

  • Speciation – the evolutionary process leading to the multiplication of species and generating biodiversity.

  • Chromosomal speciation – the theory asserting that chromosomal rearrangements cause reproductive isolation between populations and lead to speciation.

  • Peripatric speciation – the origin of a new species by budding from a parental species established beyond the periphery of the parental species range.

  • Sympatric speciation – speciation without geographic (spatial) isolation; the origin of a new species within a deme.

  • Polyploidy – the condition in which the number of chromosomes is an integral greater than two of the haploid numbers.

  • Biological species concept (BSC) – defines species as groups of interbreeding natural populations that are reproductively (genetically) isolated from other such groups.

  • Allopatric speciation – the evolution of a population into a separate species involving a period of geographic isolation.

  • The evolutionary divergence of a single phyletic line into different niches or adaptive zones.

Keywords: speciation; species concept; chromosomal rearrangements; post‐mating reproductive isolation; Spalax ehrenbergi; mole rats

Figure 1.

Geographic distribution in Israel of the four chromosomal species belonging to the S. ehrenbergi superspecies that are separated by narrow hybrid zones (2n=52, 54, 58 and 60 now called S. galili, S. golani, S. carmeli and S. judaei, respectively; see Nevo et al., ).

Figure 2.

Comparison between the four most common karyotypes of Spalax discussed in this article and now named as four biological species (Nevo et al., ). Metacentrics of groups B ‘Robertsonian chromosomes’ and C ‘inversion chromosomes’ in boxes. Acrocentrics were arbitrarily assigned to groups B and C. Reproduced with permission from Wahrman et al..

Figure 3.

Geographic distribution and karyotypes of sampling localities (*) of subterranean mole rats in Turkey. Karyotypes are represented by their circled diploid number (2n); when two localities have the same karyotype and are geographically and genetically distant, they are designated with East (E), Central (C) or West (W), 54W, 54E, 52W, 52E, 50W, 50E, 60W and 60E, which are considered here as good biological species (From Nevo et al., ).

Figure 4.

Karyotypic evolution of all karyotypes of S. leucodon superspecies (2n=38, 40, 50, 54, 60 and 62) and S. ehrenbergi superspecies (2n=52, 54, 56, 58 and 60); the two karyotypes 2n=54 and 60 are from Israel (Nevo, ). The ecological trend across which speciation presumably proceeded in both Israel and Turkey is from mesic to xeric environments, in accordance with increased aridity stress and climatic unpredictability. Rb, Robertsonian from Nevo et al., where detailed elaboration of the karyotype evolution as a function of aridity stress is presented (From Nevo et al., ).

close

References

Ayala D, Fontaine MC, Cohuet A et al. (2011) Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus. Molecular Biology Evolution 28: 745–758.

Ayala FJ and Fitch WM (1997) Genetics and the origin of species: from Darwin to molecular biology 60 years after Dobzhansky, Washington, DC. Proceedings of the National Academy of Sciences of the USA 94: 7691–7697.

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

Bakloushinskaya I, Romanenko SA, Graphodatsky AS et al. (2010) The role of chromosome rearrangements in the evolution of mole voles of the genus Ellobius (Rodentia, Mammalia). Russian Journal of Genetics 46: 1143–1145.

Basset P, Yannic G, Brunner H and Hausser J (2006) Restricted gene flow at specific parts of the shrew genome in chromosomal hybrid zones. Evolution 60: 1718–1730.

Belyayev A, Raskina O and Nevo E (2001) Evolutionary dynamics and chromosomal distribution of repetitive sequence chromosomes of Aegilops speltoides revealed by genomic in situ hybridization. Heredity 86: 738–742.

Belyayev A, Raskina O and Nevo E (2003) Evolutionary dynamics of repetitive DNA fraction in two wild Triticeae species. In: Sharma AK and Sharma A (eds) Plant Genome: Biodiversity and Evolution, vol. 1, Part A – Phanerogams, pp. 37–56. Enfield, USA: Science Publishers, Inc.

Britton‐Davidian J, Nadeau JH, Croset H and Thaler L (1989) Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty). Genetics Research 53: 29–44.

Britton‐Davidian J and Searle JB (eds) (2005) The genus Mus as a model for evolutionary studies. Biological Journal of the Linnean Society 84: 321–674.

Brown JD and O'Neill RJ (2010) Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annual Review of Genomics and Human Genetics 11: 291–316.

Capanna E (1982) Robertsonian numerical variation in animal speciation: Mus musculus, an emblematic model. In: Barigozzi C (ed.) Mechanisms of Speciation, pp. 155–177. New York: Alan R Liss.

Carson HL (1999) Selection, Darwinian fitness and evolution in local populations. In: Wasser SP (ed.) Evolutionary Theory and Processes: Modern Perspectives, Papers in Honour of Eviatar Nevo, pp. 23–30. Dordrecht, Netherlands: Kluwer Academic.

Catzeflis FM, Nevo E, Ahlquist JE and Sibley CG (1989) Relationships of the chromosomal species in the Eurasian mole rats of the Spalax ehrenbergi Group as determined by DNA–DNA hybridization, and an estimate of the spalacid‐murid divergence time. Journal of Molecular Evolution 29: 223–232.

Charlesworth B (2003) The origin of species, revisited. Genetics Research 82: 152–153.

Chung KS, Weber JA and Hipp AL (2011) Dynamics of chromosome number and genome size variation in a cytogenetically variable sedge (Carex scoparia var. scoparia, Cyperaceae). American Journal of Botany 98: 122–129.

Coyne JA and Orr HA (1998) The evolutionary genetics of speciation. Philosophical Transactions of Royal Society of London B 353: 287–305.

Coyne JA and Orr HA (2004) Speciation. Massachusetts, USA: Sinauer Associates, Inc.

Darwin C (1859) On the Origin of Species by Means of Natural Selection. London: Murray.

Dobzhansky T (1937 [1941, 1951]) Genetics and the Origin of Species, 1st, 2nd and 3rd edn. New York: Columbia University Press.

Dobzhansky T, Ayala FJ, Stebbins GL and Valentine JW (1977) Evolution. San Francisco, CA: Freeman.

Duke Becker SE, Thomas R, Trifonov VA et al. (2011) Anchoring the dog to its relatives reveals new evolutionary breakpoints across 11 species of the Canidae and provides new clues for the role of B chromosomes. Chromosome Research 19: 685–708.

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

Feder JL and Nosil P (2009) Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution 63: 3061–2075.

Forsdyke DR (2001) The Origin of Species, Revisited. Montreal: McGill‐Queens University Press.

Forsdyke DR (2004) Chromosomal speciation: a reply. Journal of Theoretical Biology 230: 189–196.

Futuyma DJ and Mayer GC (1980) Non‐allopatric speciation in animals. Systematic Zoology 29: 254–271.

Gavrilets S (2004) Fitness Landscapes and the Origin of Species. Princeton: Princeton University Press.

Grant V (1991) The Evolutionary Process. A Critical Study of Evolutionary Theory, 2nd edn. New York: Columbia University Press.

Hadid Y, Nemeth A, Snir S et al. (2012) Is evolution of blind mole rats determined by climate oscillations. PloS ONE 7(1): e30043.

Hegyi H and Tompa P (2012) Increased structural disorder of proteins encoded on human sex chromosomes. Molecular Biosystems 8: 229–236.

Howard DJ and Berlocher SH (1998) Endless Forms: Species and Speciation. Oxford: Oxford University Press.

Ivanitskaya E, Rashkovetsky L and Nevo E (2010) Chromosomes in a hybrid zone of Israeli mole rats (Spalax, Rodentia). Russian Journal of Genetics 46: 1149–1151.

Jaquiéry J, Stoeckel S, Rispe C et al. (2012) Accelerated evolution of sex chromosomes in aphids, an XO system. Molecular Biology and Evolution 29(2): 837–847.

Key KHL (1981) Species, parapatry, and the morabine grasshoppers. Systematic Zoology 30: 425–458.

King M (1993) Species Evolution. The Role of Chromosome Change. Cambridge: Cambridge University Press.

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

Kliman RM, Rogers BT and Noor MA (2001) Differences in (G+C) content between species: a commentary on Forsdyke's ‘chromosomal viewpoint of speciation’. Journal of Theoretical Biology 209: 131–140.

Kroemer JA, Nusawardani T, Rausch MA, Moser SE and Hellmich RL (2011) Transcript analysis and comparative evaluation of shaker and slowmo gene homologues from the European corn borer, Ostrinia nubilalis. Insect Molecular Biology 20(4): 493–506.

Kulathinal RJ, Stevison LS and Noor MAF (2009) The genomics of speciation in Drosophila, and introgression estimated using low‐coverage genome sequencing. PloS Genetics 5: e1000550.

Larkin DM, Pape C, Donthu R et al. (2011) Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Research 19: 770–777.

Liu S, Hui TH, Tan SL and Hong Y (2012) Chromosome evolution and genome miniaturization in minifish. PloS ONE 7: E37305.

Lowry DB and Willis JH (2010) A widespread chromosomal inversion polymorphism contributes to a major life‐history transition, local adaptation, and reproductive isolation. PloS Biology 8: e1000500.

Mank JE (2012) Small but mighty: the evolutionary dynamics of W and Y sex chromosomes. Chromosome Research 20: 21–33.

Manoukis NC, Powell JR, Toure' MB et al. (2008) A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proceedings of the National Academy of Sciences of the USA 105: 2940–2945.

Mayr E (1963) Animal Species and Evolution. Cambridge, MA: Harvard, University Press.

Michailova P, Warchalowska‐Sliwa E, Szarek‐Gwiazda E and Kownacki A (2012) Does biodiversity of macroinvertebrates and genome response of Chironomidae larvae (Diptera) reflect heavy metal pollution in a small pond? Environmental Monitoring and Assessment 184: 1–14.

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

Nevo E (1985) Speciation in action and adaptation in subterranean mole rats: patterns and theory. Bollettino di Zoologia 52: 65–95.

Nevo E (1991) Evolutionary theory and processes of active speciation and adaptive radiation in subterranean mole rats, Spalax ehrenbergi superspecies in Israel. Evolutionary Biology 25: 1–125.

Nevo E (1999) Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford: Oxford University Press.

Nevo E (2006) ‘Evolution Canyon’: a microcosm of life's evolution focusing on adaptation and speciation. Israel Journal of Ecology and Evolution 52: 485–506.

Nevo E and Bar‐El H (1976) Hybridization and speciation in fossorial mole rats. Evolution 30: 831–840.

Nevo E, Filippucci MG, Redi CD, Korol A and Beiles A (1994) Chromosomal speciation and adaptive radiation of mole rats in Asia Minor correlated with increased ecological stress. Proceedings of the National Academy of Sciences of the USA 91: 8160–8164.

Nevo E, Ivanitskaya E and Beiles A (2001) Adaptive Radiation Of Blind Subterranean Mole Rats: Naming And Revisiting the Four Sibling Species of the Spalax ehrenbergi Superspecies in Israel: Spalax galili (2n=52), S. golani (2n=54), S. carmeli (2n=58) and S. judaei (2n=60). Leiden, the Netherlands: Backhuys Publishers.

Nevo E, Ivanitskaya E, Filippucci MG and Beiles A (2000) Speciation and adaptive radiation of subterranean mole rats, Spalax ehrenbergi superspecies, in Jordan. Biological Journal of the Linnean Society 69: 263–281.

Nevo E, Kirzhner VM, Beiles A and Korol AB (1997) Selection versus random drift: long‐term polymorphism persistence in small populations (evidence and modelling). Philosophical Transactions of Royal Society of London B 352: 381–389.

Nevo E, Simson S, Heth G, Redi C and Filippucci G (1991) Recent speciation of subterranean mole rats of the Spalax ehrenbergi superspecies in the El‐Hamam isolate, northern Egypt. (Abstract). 6th Intern. Colloquium on the Ecology and Taxonomy of Small African Mammals, p. 43. August 11–16, 1991. Israel: Mitzpe Ramon.

Noor MA, Garfield DA, Schaeffer SW and Machado CA (2007) Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. Genetics 177: 1417–1428.

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.

Noor MAF and Coyne JA (2006) Speciation in the new millennium: What's left to know? In: Nevo E (ed.) New Horizons in Evolutionary Biology. Israel Journal of Ecology and Evolution 52: 431–442.

O'Neill RJW, O'Neill MJ and Graves JAM (1998) Undermethylation associated with retroelement activation and chromosome remodeling in an interspecific mammalian hybrid. Nature 393: 68–72.

Orr HA, Madden LD, Coyne JA, Goodwin R and Hawley RS (1997) The developmental genetics of hybrid inviability. A mitotic defect in Drosophila hybrids. Genetics 145: 1031–1040.

Polyakov A, Beharav A, Avivi A and Nevo E (2003) Mammalian microevolution in action: adaptive edaphic genomic divergence in blind subterranean mole rats. Proceedings Royal Society London, Biological Letters 271: S156–S159.

Pontig C (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends in Genetics 27: 165.

Redi CA and Capanna E (1988) Robertsonian heterozygotes in the mouse and the fate of their germ cells. In: Daniel A (ed.) The Cytogenetics of Mammalian Autosomal Rearrangements, pp 315–359. New York: Alan R. Liss.

Redi CA, Garagna S and Zuccotti M (1990) Robertsonian chromosome formation and fixation: the genomic scenario. Biological Journal of the Linnean Society 41: 235–255.

Riesberg LH (2001) Polyploid evolution : keeping the peace at genomic reunions. Current Biology 11: R925–R928.

Riesberg 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: 713–727.

Sharma KS, Mehra P, Kumari J et al. (2012) Physical localization and probable transcriptional activity of 18S‐5.8S‐26S rRNA gene loci in some Asiatic Cymbidiums (Orchidaceae) from north‐east India. Gene 499: 362–366.

Sin HS, Ichijima Y, Koh E et al. (2012) Human postmeiotic sex chromatin and its impact on sex chromosome evolution. Genome Research 22: 827–836.

Strasburg JL, Scotti‐Saintagne C, Scotti I, Lai Z and Rieseberg H (2009) Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Molecular Biology Evolution 26: 1341–1355.

Tore EO, Hermansen J, Fijarczyk A et al. (2011) Hybrid speciation in sparrows II: a role for sex chromosomes. Molecular Ecology 20: 3823–3837.

della Torre A, Costantini C, Besansky MJ et al. (2002) Speciation within Anapheles gambiae – the glass is half full. Science 298: 115.

Wahrman J, Richler C, Gamperl R and Nevo E (1985) Revisiting Spalax: mitotic and meiotic chromosome variability. Israel Journal of Zoology 33: 15–38.

White MJD (1978) Modes of Speciation. San Francisco, CA: Freeman.

Wu CI and Ting CT (2004) Genes and speciation. Nature Reviews Genetics 5: 114–122.

Zhang J, Wang X and Podlaha O (2012) Testing the chromosomal speciation hypothesis for humans and chimpanzees. Genome Research 14: 845–851.

Further Reading

Henry RJ (ed.) (2005) Plant Diversity and Evolution. Cambridgre, MA: CABI Publishing.

Hoffman AA and Parsons PA (1991) Evolutionary Genetics and Environmental Stress. Oxford: Oxford University Press.

Nevo E (ed.) (2006) New horizons in evolutionary biology. Israel Journal of Ecology and Evolution 52: 209–555.

Nevo E and Beiles W (2011) Genetic variation in nature. Scholarpedia 6(7): 8821.

Parisi V, De Fonzo V and Aluffi‐Pentini F (eds) (2004) Dynamical Genetics. Kerala, India: Research Signpost.

Shapiro JA (2011) Evolution. A view from the 21st century. New Jersey: FT Press Science.

Templeton AR (2006) Population Genetics and Microevolutionary Theory. New Jersey: John Wiley and Sons.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Nevo, Eviatar(Dec 2012) Speciation: Chromosomal Mechanisms. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001757.pub3]