Hybridization, introgression, and linkage evolution

Genetic mapping methods provide a unique opportunity to study the interactions of differentiated genes and genomes in a hybrid genetic background. After a brief discussion of theoretical and analytical concerns, we review the application of these methods to a wide range of evolutionary issues. Map-based studies of experimental hybrids indicate that most postzygotic reproductive barriers in plants are polygenic and that the expression of extreme or novel traits in segregating hybrids (transgressive segregation) results from the complementary action of divergent parental alleles. However, genetic studies of hybrid vigor do not concur in their interpretations of the relative roles of dominance, overdominance, and epistasis. Map-based studies of natural hybrids are much rarer, but the few existing studies confirm the polygenic basis of postzygotic barriers and demonstrate the utility of genetic linkage for detecting cryptic introgression. In addition, studies of experimental and natural hybrid lineages provide compelling evidence that homoploid hybrid speciation has occurred in nature, and that it represents a rapid and repeatable mode of speciation. Data further indicate that this mode is facilitated by strong fertility selection and high chromosomal mutation rates. We recommend that future studies of hybrid genomes focus on natural hybrids, not only because of the paucity of data in this area, but also because of the availability of highly recombinant hybrid genotypes in hybrid zones. Of particular value will be studies of long-lived or difficult-to-propagate organisms, which previously have not been amenable to genetic study.

[1]  W. D. Hanson Early Generation Analysis of Lengths of Heterozygous Chromosome Segments around a Locus Held Heterozygous with Backcrossing or Selfing. , 1959, Genetics.

[2]  M. Yano,et al.  Detection of segregation distortions in an indica-japonica rice cross using a high-resolution molecular map , 1996, Theoretical and Applied Genetics.

[3]  H. T. Stalker,et al.  Introgression analysis of an interspecific hybrid population in peanuts (Arachis hypogaea L.) using RFLP and RAPD markers. , 1995, Genome.

[4]  J. Clausen,et al.  Genetic structure of ecological races , 1958 .

[5]  K. Lark,et al.  Determining the linkage of quantitative trait loci to RFLP markers using extreme phenotypes of recombinant inbreds of soybean (Glycine max L. Merr.) , 1993, Theoretical and Applied Genetics.

[6]  Loren H. Rieseberg,et al.  Hybrid Origins of Plant Species , 1997 .

[7]  Loren H. Rieseberg,et al.  lntrogression and Its Consequences in Plants , 1993 .

[8]  D. Zamir,et al.  Genetic mapping of an ancient translocation in the genus Lens , 1987, Theoretical and Applied Genetics.

[9]  R. Fisher The theory of inbreeding , 1949 .

[10]  A. Mujeeb-Kazi,et al.  Visualization of Secale cereale DNA in wheat germ plasm by fluorescent in situ hybridization , 1995, Theoretical and Applied Genetics.

[11]  J. Weller Mapping and analysis of quantitative trait loci in Lycopersicon (tomato) with the aid of genetic markers using approximate maximum likelihood methods , 1987, Heredity.

[12]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[13]  W. E. Ritter AS TO THE CAUSES OF EVOLUTION. , 1923, Science.

[14]  A. Leitch,et al.  In Situ Localization of Parental Genomes in a Wide Hybrid , 1989 .

[15]  J. Coyne Speciation in Action , 1996, Science.

[16]  M. Soller,et al.  Linkage analysis of quantitative traits in an interspecific cross of tomato (lycopersicon esculentum x lycopersicon pimpinellifolium) by means of genetic markers. , 1988, Genetics.

[17]  S. Tanksley,et al.  Restriction fragment length polymorphism maps and the concept of graphical genotypes , 2004, Theoretical and Applied Genetics.

[18]  Y. Sano,et al.  REPRODUCTIVE BARRIERS DISTRIBUTED IN MELILOTUS SPECIES AND THEIR GENETIC BASES , 1978 .

[19]  M. Lorieux,et al.  Mapping genetic factors controlling pollen viability in an interspecific cross in Helianthus sect. Helianthus , 1995, Theoretical and Applied Genetics.

[20]  S. Tanksley,et al.  QTL analysis of transgressive segregation in an interspecific tomato cross. , 1993, Genetics.

[21]  V. Grant The regulation of recombination in plants. , 1958, Cold Spring Harbor symposia on quantitative biology.

[22]  R. Wing,et al.  FISH of a maize sh2-selected sorghum BAC to chromosomes of Sorghum bicolor. , 1997, Genome.

[23]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[24]  J. Clausen,et al.  Experimental studies on the nature of species. IV. Genetic structure of ecological races. , 1959 .

[25]  W. Anderson,et al.  A theoretical assessment of recombinational speciation , 1995, Heredity.

[26]  Cai-guo Xu,et al.  Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Baird A SIMULATION STUDY OF MULTILOCUS CLINES , 1995, Evolution; international journal of organic evolution.

[28]  K. Ritland Inferring the genetic basis of inbreeding depression in plants. , 1996, Genome.

[29]  L. Rieseberg,et al.  The effects of mating design on introgression between chromosomally divergent sunflower species , 1996, Theoretical and Applied Genetics.

[30]  A. Grootjans,et al.  Hybridization of the habitat in disturbed hay meadows , 1987 .

[31]  A. Templeton Cladistic approaches to identifying determinants of variability in multifactorial phenotypes and the evolutionary significance of variation in the human genome. , 2007, Ciba Foundation symposium.

[32]  V. Grant Selection for vigor and fertility in the progeny of a highly sterile species hybrid in gilia. , 1966, Genetics.

[33]  R. Harrison,et al.  Hybrid zones: windows on evolutionary process. , 1990 .

[34]  H. Kato,et al.  Two new loci for hybrid sterility in cultivated rice (Oryza sativa L.) , 1996, Theoretical and Applied Genetics.

[35]  Loren H. Rieseberg,et al.  Hybrid speciation accompanied by genomic reorganization in wild sunflowers , 1995, Nature.

[36]  C. Pigott Genetics and the Origin of Species , 1959, Nature.

[37]  K. Daly,et al.  DISCRETE POPULATIONS DERIVED BY INTERSPECIFIC HYBRIDIZATION AND SELECTION IN NICOTIANA , 1959 .

[38]  S. Pinson,et al.  Identification of quantitative trait loci (QTLs) for heading date and plant height in cultivated rice (Oryza sativa L.) , 1995, Theoretical and Applied Genetics.

[39]  M. Arnold,et al.  GENETIC INTERACTIONS AND NATURAL SELECTION IN LOUISIANA IRIS HYBRIDS , 1998, Evolution; international journal of organic evolution.

[40]  P. Umaharan,et al.  Inheritance of foliar resistance to Phytophthora palmivora (butler) Butler in cacao (theobroma cacao L.) , 1997, Euphytica.

[41]  D. Shaw,et al.  Response in Genotypic and Breeding Value to a Single Generation of Divergent Selection for Fresh Fruit Color in Strawberry , 1995 .

[42]  S. Barnes,et al.  Molecular marker analysis of Helianthus annuus L. 2. Construction of an RFLP linkage map for cultivated sunflower , 1995, Theoretical and Applied Genetics.

[43]  J. Doebley,et al.  Isoenzymatic Variation in Zea (Gramineae) , 1984 .

[44]  D. Gerstel A New Lethal Combination in Interspecific Cotton Hybrids. , 1954, Genetics.

[45]  L. Hollingshead,et al.  A Lethal Factor in Crepis Effective Only in an Interspecific Hybrid. , 1930, Genetics.

[46]  L. Rieseberg Genetic Mapping as a Tool for Studying Speciation , 1998 .

[47]  J. Avise,et al.  Pleistocene phylogeographic effects on avian populations and the speciation process , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  Loren H. Rieseberg,et al.  Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids , 1996, Science.

[49]  A. Paterson,et al.  The distribution of Gossypium hirsutum chromatin in G. barbadense germ plasm: molecular analysis of introgressive plant breeding , 1995, Theoretical and Applied Genetics.

[50]  W. Powell,et al.  Introgression of quantitative trait loci (QTLs) determining stripe rust resistance in barley: an example of marker-assisted line development , 1998, Theoretical and Applied Genetics.

[51]  R. Lande,et al.  Simulation of marker assisted selection for non-additive traits. , 1994, Genetical research.

[52]  C. Rick,et al.  Novel Variation in Tomato Species Hybrids , 1953, The American Naturalist.

[53]  U. Lagercrantz,et al.  Comparative genome mapping in Brassica. , 1996, Genetics.

[54]  Craig Moritz,et al.  Chromosomal Evolution and Speciation Revisited , 1987 .

[55]  G. Stebbins Experimental Studies on the Nature of Species. Volume V: Biosystematics, Genetics, and Physiological Ecology of the Erythranthe Section of Mimulus.William M. Hiesey , Malcolm A. Nobs , Olle Bjorkman , 1972 .

[56]  A. Paterson,et al.  Genetics of Hybrid Sterility and Hybrid Breakdown in an Intersubspecific Rice ( O y a sativa L.) Population , 2022 .

[57]  C. Wu,et al.  Genetics of postmating reproductive isolation in animals. , 1994, Annual review of genetics.

[58]  K. Lark,et al.  Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean (Glycine max L.) , 1993, Theoretical and Applied Genetics.

[59]  P. Sniegowski,et al.  The fertility effects of pericentric inversions in Drosophila melanogaster. , 1993, Genetics.

[60]  L. Rieseberg,et al.  INTERSPECIFIC POLLEN COMPETITION AS A REPRODUCTIVE BARRIER BETWEEN SYMPATRIC SPECIES OF HELIANTHUS (ASTERACEAE) , 1995 .

[61]  W. D. Hanson The Breakup of Initial Linkage Blocks under Selected Mating Systems. , 1959, Genetics.

[62]  B. Carver,et al.  Genetic analysis of photosynthetic variation in hexaploid and tetraploid wheat and their interspecific hybrids , 1989, Photosynthesis Research.

[63]  I. Leitch,et al.  The use of genomic in situ hybridization (GISH) to show transmission of recombinant chromosomes by a partially fertile bigeneric hybrid, Gasteria lutzii ×Aloe aristata (Aloaceae), to its progeny , 1997, Chromosoma.

[64]  C. Jan,et al.  Chromosomal Differentiation among the Annual Helianthus Species , 1986 .

[65]  N. Barton,et al.  THE GENETIC STRUCTURE OF THE HYBRID ZONE BETWEEN THE FIRE‐BELLIED TOADS BOMBINA BOMBINA AND B. VARIEGATA: COMPARISONS BETWEEN TRANSECTS AND BETWEEN LOCI , 1991, Evolution; international journal of organic evolution.

[66]  F. Ayala Molecular systematics , 2004, Journal of Molecular Evolution.

[67]  M. Macnair,et al.  Complementary lethal factors in two North American populations of the yellow monkey flower , 1984 .

[68]  M. Daly,et al.  MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. , 1987, Genomics.

[69]  W. Hollander,et al.  Introgressive Hybridization , 1949, The Yale Journal of Biology and Medicine.

[70]  R. Fisher,et al.  A fuller theory of “Junctions” in inbreeding , 1954, Heredity.

[71]  B. Gill,et al.  Detection of barley chromatin added to wheat by genomic in situ hybridization , 1991 .

[72]  D. Brar,et al.  Alien introgression in rice , 1997, Plant Molecular Biology.

[73]  Keith A. Gardner,et al.  Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. , 1999, Genetics.

[74]  K. Devos,et al.  The effect of genome and sex on recombination rates in Pennisetum species , 1996, Theoretical and Applied Genetics.

[75]  N. Barton,et al.  Analysis of Hybrid Zones , 1985 .

[76]  L. Gottlieb,et al.  Genetic studies of the pattern of floral pigmentation in Clarkia gracilis , 1988, Heredity.

[77]  C. Heiser HYBRIDIZATION IN THE ANNUAL SUNFLOWERS: HELIANTHUS ANNUUS x H. DEBILIS VAR. CUCUMERIFOLIUS , 1951 .

[78]  E S Lander,et al.  Restriction fragment length polymorphism linkage map for Arabidopsis thaliana. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[79]  J. Li,et al.  Identification of QTLs affecting traits of agronomic importance in a recombinant inbred population derived from a subspecific rice cross , 1996, Theoretical and Applied Genetics.

[80]  L. Rieseberg,et al.  Genomic map of a diploid hybrid species , 1993, Heredity.

[81]  C. Cockerham,et al.  Design III with marker loci. , 1996, Genetics.

[82]  J. Whittaker,et al.  Using marker-maps in marker-assisted selection. , 1995, Genetical research.

[83]  H. Oka Analysis of genes controlling f(1) sterility in rice by the use of isogenic lines. , 1974, Genetics.

[84]  L. Rieseberg,et al.  Long-term introgression of crop genes into wild sunflower populations , 1998, Theoretical and Applied Genetics.

[85]  F. Hospital,et al.  More on the efficiency of marker-assisted selection , 1997, Theoretical and Applied Genetics.

[86]  R. Lande,et al.  Efficiency of marker-assisted selection in the improvement of quantitative traits. , 1990, Genetics.

[87]  R. Lande,et al.  Simulation of marker assisted selection in hybrid populations. , 1994, Genetical research.

[88]  S. Tanksley,et al.  RFLP analysis of the size of chromosomal segments retained around the Tm-2 locus of tomato during backcross breeding , 1989, Theoretical and Applied Genetics.

[89]  S. Tanksley,et al.  Molecular Mapping of Plant Chromosomes , 1988 .

[90]  V. Grant Genetics of Flowering Plants , 1976 .

[91]  N. Barton MULTILOCUS CLINES , 1983, Evolution; international journal of organic evolution.

[92]  R. Lande,et al.  Marker-assisted selection and marker-QTL associations in hybrid populations , 1995, Theoretical and Applied Genetics.

[93]  M. Slatkin,et al.  Segregation variance after hybridization of isolated populations. , 1994, Genetical research.

[94]  L. Rieseberg,et al.  Introgression between the Cultivated Sunflower and a Sympatric Wild Relative, Helianthus petiolaris (Asteraceae) , 1999, International Journal of Plant Sciences.

[95]  J. True,et al.  A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. , 1996, Genetics.

[96]  W. Ewens Genetics and analysis of quantitative traits , 1999 .

[97]  W. J. Libby,et al.  Maintenance of a Lethal in a Natural Population of Mimulus guttatus , 1972, The American Naturalist.

[98]  M. Arnold Natural Hybridization and Evolution , 1997 .

[99]  M. Byrne,et al.  An integrated genetic linkage map for eucalypts using RFLP, RAPD and isozyme markers , 1995, Theoretical and Applied Genetics.

[100]  A. Templeton MECHANISMS OF SPECIATION­ A POPULATION GENETIC APPROACH , 1981 .

[101]  E. Lander,et al.  Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. , 1992, Genetics.

[102]  D. Zamir,et al.  Unequal Segregation of Nuclear Genes in Plants , 1986, Botanical Gazette.

[103]  N. Barton,et al.  The genetic basis of hybrid inviability in the grasshopper Podisma pedestris , 1981, Heredity.

[104]  Chung-I Wu,et al.  Haldane's rule and its legacy: Why are there so many sterile males? , 1996, Trends in ecology & evolution.

[105]  O. Kempthorne,et al.  Proceedings of the International Conference on Quantitative Genetics. , 1978 .

[106]  C. Guenther,et al.  RFLP analysis of chromosomal segregation in progeny from an interspecific hexaploid somatic hybrid between Solanum brevidens and Solanum tuberosum. , 1993, Genetics.

[107]  L. Gottlieb,et al.  GENE DUPLICATION AND PHYLOGENY IN CLARKIA , 1979, Evolution; international journal of organic evolution.

[108]  J. Bennett Junctions in inbreeding , 2005, Genetica.

[109]  John L. Strother,et al.  Flora Novo-Galiciana. 12. Compositae. , 1986 .

[110]  L. Rieseberg,et al.  Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[111]  P. Lu,et al.  Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[112]  S. Bennett,et al.  Genomic in situ hybridization reveals the allopolyploid nature ofMilium montianum (Gramineae) , 1992, Chromosoma.

[113]  C. Stuber,et al.  Characterization of a Yield Quantitative Trait Locus on Chromosome Five of Maize by Fine Mapping , 1997 .

[114]  S. G. Stephens The Cytogenetics of Speciation in Gossypium. I. Selective Elimination of the Donor Parent Genotype in Interspecific Backcrosses. , 1949, Genetics.

[115]  G. Ledyard Stebbins,et al.  Variation and Evolution in Plants , 1951 .

[116]  M. Mutschler,et al.  Marker-assisted transfer of acylsugar-mediated pest resistance from the wild tomato, Lycopersicon pennellii, to the cultivated tomato, Lycopersicon esculentum , 1997, Molecular Breeding.

[117]  Loren H. Rieseberg,et al.  What can molecules and morphological markers tell us about plant hybridization , 1993 .

[118]  S. Tanksley,et al.  Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines , 1996, Theoretical and Applied Genetics.

[119]  G. Stebbins,et al.  The inviability, weakness, and sterility of interspecific hybrids. , 1958, Advances in genetics.

[120]  P. Lichter,et al.  Mapping and chromosome analysis: the potential of fluorescence in situ hybridization. , 1994, Journal of biotechnology.

[121]  M V Olson,et al.  Physical map of the Saccharomyces cerevisiae genome at 110-kilobase resolution. , 1991, Genetics.

[122]  R. Lewontin,et al.  HYBRIDIZATION AS A SOURCE OF VARIATION FOR ADAPTATION TO NEW ENVIRONMENTS , 1966, Evolution; international journal of organic evolution.

[123]  D. Charlesworth Hybrid Speciation: Evolution under the microscope , 1995, Current Biology.

[124]  J. McGrath,et al.  Segregation and recombination of Solanum brevidens synteny groups in progeny of somatic hybrids with S. tuberosum: intragenomic equals or exceeds intergenomic recombination. , 1996, Genetics.

[125]  C. Chevalet,et al.  Using markers in gene introgression breeding programs. , 1992, Genetics.

[126]  V. Grant The origin of a new species of gilia in a hybridization experiment. , 1966, Genetics.

[127]  M. Macnair,et al.  Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus? , 1983, Heredity.

[128]  S. Tanksley,et al.  Isozymic gene linkage map of the tomato: Applications in genetics and breeding , 1980, Theoretical and Applied Genetics.

[129]  T. Mitchell-Olds,et al.  Interval mapping of viability loci causing heterosis in Arabidopsis. , 1995, Genetics.

[130]  G. Khush,et al.  RFLP analysis of rice (Oryza sativa L.) introgression lines , 1992, Theoretical and Applied Genetics.

[131]  L. Rieseberg,et al.  Chromosomal and genic barriers to introgression in Helianthus. , 1995, Genetics.

[132]  S. Tanksley,et al.  Introgression and DNA marker analysis of Lycopersicon peruvianum, a wild relative of the cultivated tomato, into Lycopersicon esculentum, followed through three successive backcross generations , 1997, Theoretical and Applied Genetics.

[133]  L. Gentzbittel,et al.  Development of a consensus linkage RFLP map of cultivated sunflower (Helianthus annuus L.) , 1995, Theoretical and Applied Genetics.

[134]  A. Graner,et al.  Localization of quantitative trait loci (QTL) for agronomic important characters by the use of a RFLP map in barley (Hordeum vulgare L.) , 1995, Theoretical and Applied Genetics.

[135]  T. Helentjaris,et al.  Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. , 1988, Genetics.

[136]  L. Rieseberg,et al.  Rapid hybrid speciation in wild sunflowers. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[137]  D. Erwin,et al.  New approaches to speciation in the fossil record , 1995 .

[138]  J. Hermsen The genetic basis of hybrid necrosis in wheat , 1963, Genetica.