Abstract
Over the past decade several theoretical and empirical studies have revived interest in the role of chromosomes in speciation. The resulting models do not suffer from the problems experienced by previously proposed mechanisms of chromosomal speciation, because they invoke suppression of recombination rather than a reduction in the fitness of heterokaryotypes as their core process. However, they are not free from difficulties. The evidence for recombination-suppression models is discussed here. The general conclusion is that a consensus opinion on which models best describe the real-world situation is currently unlikely because of an inability of the available empirical evidence to fully distinguish between them, which may be due in part to a lack of exclusivity. I argue that future work should take this lack of exclusivity into account. Resolving the biogeography of speciation is also suggested in order to tell the various models apart. Further study is needed which focuses on confirming the operation of individual elements of the various models, rather than attempting to validate any single mechanism as a whole.


Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, Drosophila and mosquitoes. Proc Natl Acad Sci USA 102:6535–6542
Brown KM, Burk LM, Henagan LM, Noor MAF (2004) A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura. Evolution 58:1856–1860
Bush GL, Case SM, Wilson AC, Patton JL (1977) Rapid speciation and chromosomal evolution in mammals. Proc Natl Acad Sci USA 74:3942–3946
Butlin RK (2005) Recombination and speciation. Mol Ecol 14:2621–2635
Butlin RK, Galindo J, Grahame JW (2008) Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos Trans R Soc B 363:2997–3007
Chang AS, Noor MAF (2007) The genetics of hybrid male sterility between the allopatric species pair Drosophila persimilis and D. pseudoobscura bogotana: dominant sterility alleles in collinear autosomal regions. Genetics 176:343–349
Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68:444–456
Christie P, Macnair MR (1984) Complementary lethal factors in two North American populations of the yellow monkey flower. J Hered 75:510–511
Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381
Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond Ser B 353:287–305
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland
Coyne JA, Aulard S, Berry A (1991) Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics 129:791–802
Davisson MT, Akeson EC (1993) Chromosomes in the mouse. Genetics 667:649–667
Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25:660–669
Feder JL, Nosil P (2009) Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution 63:3061–3075
Felsenstein J (1981) Scepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124–138
Fishman L, Willis JH (2001) Evidence for Dobzhansky-Muller incompatibilities contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55:1932–1942
Gavrilets S (2000) Waiting time to parapatric speciation. P R Soc B Biol Sci 267:2483–2492
Gavrilets S (2003) Perspective: models of speciation: what have we learned in 40 years? Evolution 57:2197–2215
Graubard MA (1931) Inversions in Drosophila melanogaster. Genetics 17:81–104
Hale DW (1986) Heterosynapsis and suppression of chiasmata within heterozygous pericentric inversions of the Sitka deer mouse. Chromosoma 94:425–432
Hoffmann AA, Rieseberg LH (2008) Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu Rev Ecol Evol Syst 39:21–42
Karaman MW, Houck ML, Chemnick LG, Nagpal S, Chawannakul D, Sudano D, Pike BL, Ho VV, Ryder OA, Hacia JG (2003) Comparative analysis of gene-expression patterns in Human and African great ape cultured fibroblasts. Genome Res 13:1619–1630
Khaitovich P, Muetzel B, She X, Lachmann M, Hellmann I, Dietzsch J, Steigele S, Do HH, Weiss G, Enard W et al (2004) Regional patterns of gene expression in human and chimpanzee brains. Genome Res 14:1462–1473
Kirkpatrick M, Barton N (2006) Chromosomal inversions, local adaptation, and speciation. Genetics 173:419–434
Kondrashov AS (2003) Accumulation of Dobzhansky-Muller incompatibilities within a spatially structured population. Evolution 57:151–153
Kulathinal RJ, Stevison LS, Noor MAF (2009) The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet 5:e1000550
Kumar S, Filipski A, Swarna V, Walker A, Hedges SB (2005) Placing confidence limits on the molecular age of the human-chimpanzee divergence. Proc Natl Acad Sci USA 102:18842–18847
Levin DA, Wilson AC (1976) Rates of evolution in seed plants: net increase in diversity of chromosome numbers and species numbers through time. Proc Natl Acad Sci USA 73:2086–2090
Lu J, Li W-H, Wu C-I (2003) Comment on ‘Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes’. Science 302:988
Machado CA, Haselkorn TS, Noor MAF (2007) Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D. persimilis. Genetics 175:1289–1306
Mallet J (2006) What does Drosophila genetics tell us about speciation? Trends Ecol Evol 21:386–393
Marquès-Bonet T, Caceres M, Bertranpetit J, Preuss TM, Thomas JW, Navarro A (2004) Chromosomal rearrangements and the genomic distribution of gene-expression divergence in humans and chimpanzees. Trends Genet 20:524–529
Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Columbia University Press, New York
Mikkelson et al. The Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87
Navarro A, Barton NH (2003a) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447–459
Navarro A, Barton NH (2003b) Chromosomal speciation and molecular divergence—accelerated evolution in rearranged chromosomes. Science 300:321–324
Navarro A, Bétran E, Barbadilla A, Ruiz A (1997) Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695–709
Navarro A, Barbadilla A, Ruiz A (2000) Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics 155:685–698
Navarro A, Marqués-Bonet T, Barton NH (2003) Response to comment on “Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes”. Science 302:988
Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci USA 98:12084–12088
Noor MAF, Garfield DA, Schaeffer SW, Machado CA (2007) Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. Genetics 177:1417–1428
Orr HA (1995) The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805–1813
Palopoli MF, Wu C-I (1994) Genetics of hybrid male sterility between Drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics 138:329–341
Rieseberg LH (2001) Chromosomal arrangements and speciation. Trends Ecol Evol 16:351–358
Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914
Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713–727
Schaeffer SW, Anderson WW (2005) Mechanisms of genetic exchange within the chromosomal inversions of Drosophila pseudoobscura. Genetics 171:1729–1739
Shuker DM, Underwood K, King TM, Butlin RK (2005) Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc R Soc B Biol Sci 272:2491–2497
Strasburg JL, Scotti-Saintagne C, Scotti I, Lai Z, Rieseberg LH (2009) Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Mol Biol Evol 26:1341–1355
Trickett AJ, Butlin RK (1994) Recombination suppressors and the evolution of new species. Heredity 73:339–345
White MJD (1978) Modes of speciation. Freeman, San Fransisco
Yatabe Y, Kane NC, Scotti-Santagne C, Rieseberg LH (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175:1883–1893
Acknowledgments
Thank you to Professor Roger Butlin for providing supervision during the writing of an earlier version of this manuscript as an undergraduate dissertation at the University of Sheffield, as well as for subsequent helpful discussions and advice, and to two anonymous reviewers for their comments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jackson, B.C. Recombination-suppression: how many mechanisms for chromosomal speciation?. Genetica 139, 393–402 (2011). https://doi.org/10.1007/s10709-011-9558-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-011-9558-0


