A genomic view of introgression and hybrid speciation

Current Opinion in Genetics and Development

Volumn 17, Issue 6, 2007, Pages 513-518

  Baack, Eric J ^a   Rieseberg, Loren H ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; CHROMOSOME REARRANGEMENT; GENE DELETION; GENE EXPRESSION; GENE MAPPING; GENE SILENCING; GENETIC POLYMORPHISM; GENETIC TRAIT; GENETIC VARIABILITY; GENOME; GENOME ANALYSIS; GENOMICS; HELIANTHUS ANNUUS; HELIANTHUS ARGOPHYLLUS; HELIANTHUS PETIOLARIS; HETEROSIS; HYBRIDIZATION; INTROGRESSION; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; REVIEW; SUNFLOWER;

GENETIC SPECIATION; GENOMICS; HYBRID VIGOR; HYBRIDIZATION, GENETIC;

ANIMALIA; HELIANTHUS; QUERCUS;

EID: 36549053175     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2007.09.001     Document Type: Review

References (54)

1. Linnaeus C. Systema naturae (1735), de Graaf, Neiuwkoop
2. Larson J.L. The species concept of Linnaeus. Isis 59 (1968) 291-299
3. In: Syvanen M., and Kado C. (Eds). Horizontal Gene Transfer (2002), Academic Press, San Diego
4. Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol 20 (2005) 229-237
5. Rieseberg L.H., and Wendel J.F. Introgression and its consequences in plants. In: Harrison R.G. (Ed). Hybrid Zones and the Evolutionary Process (1993), Oxford University Press 70-109
6. Muir G., and Schlotterer C. Evidence for shared ancestral polymorphism rather than recurrent gene flow at microsatellite loci differentiating two hybridizing oaks (Quercus spp.). Mol Ecol 14 (2005) 549-561
7. Lexer C., Kremer A., and Petit R.J. Shared alleles in sympatric oaks: recurrent gene flow is a more parsimonious explanation than ancestral polymorphism. Mol Ecol 15 (2006) 2007-2012
8. Scotti-Saintagne C., Mariette S., Porth I., Goicoechea P.G., Barreneche T., Bodenes K., Burg K., and Kremer A. Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168 (2004) 1615-1626
9. Sang T., and Ge S. The puzzle of rice domestication. J Integrative Plant Biol 49 (2007) 760-768
10. Kronforst M.R., Young L.G., Blume L.M., and Gilbert L.E. Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60 (2006) 1254-1268
11. Won Y.J., and Hey J. Divergence population genetics of chimpanzees. Mol Biol Evol 22 (2005) 297-307
12. Won Y.J., Sivasundar A., Wang Y., and Hey J. On the origin of Lake Malawi cichlid species: a population genetic analysis of divergence. Proc Natl Acad Sci U S A 102 (2005) 6581-6586
13. Bull V., Beltran M., Jiggins C.D., McMillan W.O., Bermingham E., and Mallet J. Polyphyly and gene flow between non-sibling Heliconius species. BMC Biol (2006) 4. In this study, four loci were sequenced from two species of butterfly, Heliconius cydno and H. melpomene, both of which occur in Panama. Two loci were reciprocally monophyletic but alleles of the other two were shared between the two species. Bayesian modeling suggests that this is because of introgression at one of the loci and ancestral polymorphism at the other.
14. Buerkle CA, Rieseberg LH: The rate of genome stabilization in homoploid hybrid species. Evolution 2007, in press.
15. Morrell P.L., Williams-Coplin T.D., Lattu A.L., Bowers J.E., Chandler J.M., and Patterson A.H. Crop-to-weed introgression has impacted allelic composition of johnsongrass populations with and without recent exposure to cultivated sorghum. Mol Ecol 14 (2005) 2143-2154
16. Linder C.R., and Rieseberg L.H. Reconstructing patterns of reticulate evolution UN plants. Am J Bot 91 (2004) 1700-1708
17. Martinsen G.D., Whitham T.G., Turek R.J., and Keim P. Hybrid populations selectively filter gene introgression between species. Evolution 55 (2001) 1325-1335
18. Macholan M., Munclinger P., Sugerkova M., Dufkova P., Bimova B., Bozikova E., Zima J., and Pialek J. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61 (2007) 746-771
19. Payseur B.A., Krenz J.G., and Nachman M.W. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58 (2004) 2064-2078
20. Machado C.A., Haselkorn T.S., and Noor M.A.F. 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 (2007) 1289-1306
21. Turner T.L., Hahn M.W., and Nuzhdin S.V. Genomic islands of speciation in Anopheles gambiae. Plos Biol 3 (2005) 1572-1578
22. Yatabe Y., Kane N.C., Scotti-Saintagne C., and Rieseberg L.H. Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and Helianthus petiolaris. Genetics 175 (2007) 1883-1893. This study looks at differentiation of coding and noncoding loci in three species of sunflower. Helianthus annuus and H. argophyllus are sister species with nonoverlapping ranges, while H. petiolaris is less closely related but overlaps extensively with H. annuus. The sister species are more differentiated genetically than two phylogenetically more distant species that occur together and hybridize. Differentiation between H. annuus and H. petiolaris ranges from zero to complete, depending on the locus examined.
23. Barton N.H. Gene flow past a cline. Heredity 43 (1979) 333-339
24. Lexer C., Buerkle C.A., Joseph J.A., Heinze B., and Fay M.F. Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98 (2007) 74-84
25. Payseur B.A., and Place M. Searching the genomes of inbred mouse strains for incompatibilities that reproductively isolate their wild relatives. J Heredity 98 (2007) 115-122
26. Rieseberg L.H., Whitton J., and Gardner K. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152 (1999) 713-727
27. Adams K.L., and Wendel J.F. Allele-specific, bidirectional silencing of an alcohol dehydrogenase gene in different organs of interspecific diploid cotton hybrids. Genetics 171 (2005) 2139-2142. Over the past decade, many studies have examined the genomic changes seen in synthesized polyploids, including changes in gene expression. It was not known whether these changes were because of hybridization or genome duplication. Adams and Wendel looked at gene expression of alcohol dehydrogenase in several tissues of diploid F1 cotton hybrids. They found that some crosses resulted in repeatable reciprocal tissue-specific expression of alternative alleles, and that these changes were not because of gene deletions. This study documents that repeatable changes in gene expression occur because of hybridization without chromosome doubling.
28. Hegarty M.J., Barker G.L., Wilson I.D., Abbott R.J., Edwards K.J., and Hiscock S.J. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16 (2006) 1652-1659
29. Levy A., and Feldman M. Genetic and epigenetic reprogramming of the wheat genome upon allopolyploidization. Biol J Linnean Soc 82 (2004) 607-613
30. Chen Z.J., and Ni Z.F. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28 (2006) 240-252
31. Karrenberg S., Lexer C., and Rieseberg L.H. Reconstructing the history of selection during homoploid hybrid speciation. Am Nat 169 (2007) 725-737
32. Lai Z., Nakazato T., Salmaso M., Burke J.M., Tang S.X., Knapp S.J., and Rieseberg L.H. Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171 (2005) 291-303
33. Baack E.J., Whitney K.D., and Rieseberg L.H. Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytologist 167 (2005) 623-630
34. Schwarzbach A.E., and Rieseberg L.H. Likely multiple origins of a diploid hybrid sunflower. Mol Ecol 11 (2002) 1703-1715
35. Ungerer M.C., Strakosh S.C., and Zhen Y. Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol 16 (2006) R872-R873. Initial studies in Drosophila found little evidence for a role for transposons in species differences. Ungerer examined copy number of a Ty3/Gypsy-like retrotransposon in three species of sunflower that originated from hybridization and the two parental species. Quantitative PCR found 5-24-fold increases in copy number in the hybrid species, accounting for 62-79% of the difference in genome size between the hybrid species and their parents.
36. Lai Z., Gross B.L., Zou Y., Andrews J., and Rieseberg L.H. Microarray analysis reveals differential gene expression in hybrid sunflower species. Mol Ecol 15 (2006) 1213-1227
37. Lippman Z.B., and Zamir D. Heterosis: revisiting the magic. Trends Genet 23 (2007) 60-66
38. Cockerham C.C., and Zeng Z.B. Design III with marker loci. Genetics 143 (1996) 1437-1456
39. Swanson-Wagner R.A., Jia Y., DeCook R., Borsuk L.A., Nettleton D., and Schnable P.S. All possible modes of gene action are observed in a global comparison of gene expression in a maize F-1 hybrid and its inbred parents. Proc Natl Acad Sci U S A 103 (2006) 6805-6810
40. Hua J.P., Xing Y.Z., Wu W.R., Xu C.G., Sun X.L., Yu S.B., and Zhang Q.F. Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A 100 (2003) 2574-2579
41. Birchler J.A., Auger D.L., and Riddle N.C. In search of the molecular basis of heterosis. Plant Cell 15 (2003) 2236-2239
42. Semel Y., Nissenbaum J., Menda N., Zinder M., Krieger U., Issman N., Pleban T., Lippman Z., Gur A., and Zamir D. Overdominant quantitative trait loci for yield and fitness in tomato. Proc Natl Acad Sci U S A 103 (2006) 12981-12986
43. Redei G.P. Single locus heterosis. Z. Vererbungsl 93 (1962) 164-170
44. Landry C.R., Wittkopp P.J., Taubes C.H., Ranz J.M., Clark A.G., and Hartl D.L. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171 (2005) 1813-1822
45. Michalak P., and Noor M.A.F. Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol 20 (2003) 1070-1076
46. Springer N.M., and Stupar R.M. Allelic variation and heterosis in maize: How do two halves make more than a whole?. Genome Res 17 (2007) 264-275
47. Facon B., Jarne P., Pointier J.P., and David P. Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18 (2005) 524-535
48. Barton N.H. The role of hybridization in evolution. Mol Ecol 10 (2001) 551-568
49. Nolte A.W., Freyhof J., Stemshorn K.C., and Tautz D. An invasive lineage of sculpins, Cottus sp (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Proc Roy Soc B: Biol Sci 272 (2005) 2379-2387
50. Schwarz D., Shoemaker K.D., Botteri N.L., and McPheron B.A. A novel preference for an invasive plant as a mechanism for animal hybrid speciation. Evolution 61 (2007) 245-256
51. Mavarez J., Salazar C.A., Bermingham E., Salcedo C., Jiggins C.D., and Linares M. Speciation by hybridization in Heliconius butterflies. Nature 441 (2006) 868-871
52. Gompert Z., Fordyce J.A., Forister M.L., Shapiro A.M., and Nice C.C. Homoploid hybrid speciation in an extreme habitat. Science 314 (2006) 1923-1925. Hybrid speciation in animals was thought to be much rarer than in plants, but recent reports are narrowing the gap. Here, genetic data document the hybrid origin of a butterfly in the genus Lycaeides. The hybrid species occupies a novel alpine habitat distinct from that of either parent.
53. Martin N.H., Bouck A.C., and Arnold M.L. Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172 (2006) 2481-2489
54. Wang J.L., Tian L., Lee H.S., and Chen Z.J. Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics 173 (2006) 965-974. One of the best studies connecting hybridization to changes in a phenotype with adaptive significance, including a detailed analysis of the genetic changes. The authors elucidate the factors leading an allotetraploid species to have a later flowering time than either of its diploid progenitors.