Introgression, also known as introgressive hybridization, in genetics is the transfer of genetic material from one species into the gene pool of another by the repeated backcrossing of an interspecific hybrid with one of its parent species. Introgression is a long-term process, even when artificial; it may take many hybrid generations before significant backcrossing occurs. This process is distinct from most forms of gene flow in that it occurs between two populations of different species, rather than two populations of the same species.
A phylogenetic model of introgressive hybridization; the hybrid zone of the two species' lineages is shown in blue, with each horizontal line representing an individual introgressive event.
Introgression also differs from simple hybridization. Simple hybridization results in a relatively even mixture; gene and allele frequencies in the first generation will be a uniform mix of two parental species, such as that observed in mules. Introgression, on the other hand, results in a complex, highly variable mixture of genes, and may only involve a minimal percentage of the donor genome.
Introgression or introgressive hybridization is the incorporation (usually via hybridization and backcrossing) of novel genes and/or alleles from one taxon into the gene pool of a second, distinct taxon.[1][2][3][4] This introgression is considered 'adaptive' if the genetic transfer results in an overall increase in the recipient taxon's fitness.[5]
Ancient introgression events can leave traces of extinct species in present-day genomes, a phenomenon known as ghost introgression.[6]
Source of variation
Introgression is an important source of genetic variation in natural populations and may contribute to adaptation and even adaptive radiation.[7] It can occur across hybrid zones due to chance, selection or hybrid zone movement.[8] There is evidence that introgression is a ubiquitous phenomenon in plants and animals,[9][10] including humans,[11] in which it may have introduced the microcephalin D allele.[12]
It has been proposed that, historically, introgression with wild animals is a large contributor to the wide range of diversity found in domestic animals, rather than multiple independent domestication events.[13]
Introgressive hybridization has also been shown to be important in the evolution of domesticated crop species, possibly providing genes that help in their expansion into different environments. A genomic study from New York University Abu Dhabi Center for Genomics and Systems Biology showed that domesticated date palm varieties from North Africa show introgressive hybridization of between 5-18% of its genome from the wild Cretan palm Phoenix theophrasti into Middle East date palms P. dactylifera. This process is also similar to the evolution of apples by hybridization of Central Asian apples with the European crabapple.[14] It has also been shown that indica rice arose when Chinese japonica rice arrived in India about ~4,500 years ago and hybridized with an undomesticated proto-indica or wild O. nivara, and transferred key domestication genes from japonica to indica.[15]
There is strong evidence for the introgression of Neanderthal genes[16] and Denisovan genes[17] into parts of the modern human gene pool.
Birds
The Mallard duck is possibly the world's most capable bird to hybridise with other duck species, often to the point of the loss of genetic identity of these species. For example, feral mallard populations have significantly reduced wild populations of the Pacific black duck in New Zealand and Australia through cross-breeding.[citation needed]
Butterflies
One important example of introgression has been observed in studies of mimicry in the butterfly genus Heliconius.[18] This genus includes 43 species and many races with different color patterns. Congeners exhibiting overlapping distributions show similar color patterns. The subspecies H. melpomene amaryllis and H. melpomene timareta ssp. nov. overlap in distribution.
Using the ABBA/BABA test, some researchers have observed that there is about 2% to 5% introgression between the pair of subspecies. Importantly, the introgression is not random. The researchers saw significant introgression in chromosomes 15 and 18, where important mimicry loci are found (loci B/D and N/Yb). They compared both subspecies with H. melpomene agalope, which is a subspecies near H. melpomene amaryllis in entire genome trees. The result of the analysis was that there is no relation between those two species and H. melpomene agalope in the loci B/D and N/Yb. Moreover, they performed the same analysis with two other species with overlapping distributions, H. timareta florencia and H. melpomene agalope. They demonstrated introgression between the two taxa, especially in the loci B/D and N/Yb.
Finally, they concluded their experiments with sliding-window phylogenetic analyses, estimating different phylogenetic trees depending on the different regions of the loci. When a locus is important in the color pattern expression, there is a close phylogenetic relationship between the species. When the locus is not important in the color pattern expression, the two species are phylogenetically distant because there is no introgression at such loci.
Domestic species
Introgression can have a significant impact on non-human populations through hybridization, for instance, between wild and domestic populations of animals. This includes household pets, as seen in cats[19] or in dogs.[20]
Introgression has been observed in several plant species. For instance, a species of iris from southern Louisiana has been studied by Arnold & Bennett (1993) regarding the increased fitness of hybrid variants.[21][22]
Fish
Espinasa et al. found that introgression between a surface-dwelling members of Astroblepus and a troglomorphic species, Astroblepus pholeter, resulted in the development of previously lost traits in offspring, such as distinct eyes and optic nerves.[23]
Introgression line
An introgression line (IL) is a crop species that contains genetic material artificially derived from a wild relative population through repeated backcrossing. An example of a collection of ILs (called an IL-Library) is the use of chromosome segments from Solanum pennellii (a wild species of tomato) that was introgressed into Solanum lycopersicum (the cultivated tomato). The lines of an IL-library usually cover the complete genome of the donor. Introgression lines allow the study of quantitative trait loci, but also the creation of new varieties by introducing exotic traits.[24]
Lineage fusion
Lineage fusion on a phylogenetic tree; individual introgression events within the hybrid zone (blue) are shown as horizontal lines. Hybrids are produced before the lineages fuse, but rejoin one of the two lineages. Neither species A nor B remains extant in the area of interest.
Lineage fusion is an extreme variant of introgression that results from the merging of two distinct species or populations. This eventually results in a single population that displaces or replaces the parental species in the region.[25] Some lineage fusion occurs soon after two taxa diverge or speciate, especially if there are few reproductive barriers between lineages. [26] It is not strictly necessary for the two lineages to be closely related, but rather have the ability to produce viable offspring.
^Anderson, Edgar; Hubricht, Leslie (1938). "Hybridization in Tradescantia. III. The Evidence for Introgressive Hybridization". American Journal of Botany. 25 (6): 396. doi:10.2307/2436413. JSTOR 2436413.
^Anderson E, 1949. Introgressive hybridization. New York: Wiley & Sons
^Harrison, R (2014). "Hybridization, Introgression, and the Nature of Species Boundaries". Journal of Heredity. 105: 795–809. doi:10.1093/jhered/esu033. PMID 25149255.
^Ottenburghs, Jente; Kraus, Robert H. S.; van Hooft, Pim; van Wieren, Sipke E.; Ydenberg, Ronald C.; Prins, Herbert H. T. (2017). "Avian introgression in the genomic era". Avian Research. 8 (1): 30. doi:10.1186/s40657-017-0088-z. ISSN 2053-7166.
^Suarez-Gonzalez, Adriana; Lexer, Christian; Cronk, Quentin C. B. (2018-03-31). "Adaptive introgression: a plant perspective". Biology Letters. 14 (3): 20170688. doi:10.1098/rsbl.2017.0688. PMC5897607. PMID 29540564.
^Grant P.R., Grant B.R., Petren K. (2005). "Hybridization in the Recent Past". The American Naturalist. 166 (1): 56–67. doi:10.1086/430331. PMID 15937789. S2CID 23841467.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^Richard Buggs (2007). "Empirical study of hybrid zone movement". Heredity. 99 (3): 301–312. doi:10.1038/sj.hdy.6800997. PMID 17611495.
^Dowling T. E.; Secor C. L. (1997). "The role of hybridization and introgression in the diversification of animals". Annual Review of Ecology and Systematics. 28: 593–619. doi:10.1146/annurev.ecolsys.28.1.593. S2CID 52367016.
^Bullini L (1994). "Origin and evolution of animal hybrid species". Trends in Ecology and Evolution. 9 (11): 422–426. doi:10.1016/0169-5347(94)90124-4. PMID 21236911.
^Holliday T. W. (2003). "Species concepts, reticulations, and human evolution". Current Anthropology. 44 (5): 653–673. doi:10.1086/377663. S2CID 85569586.
^Evans, Pd; Mekel-Bobrov, N; Vallender, Ej; Hudson, Rr; Lahn, Bt (Nov 2006). "Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage". Proceedings of the National Academy of Sciences of the United States of America. 103 (48): 18178–83. Bibcode:2006PNAS..10318178E. doi:10.1073/pnas.0606966103. ISSN 0027-8424. PMC1635020. PMID 17090677.
^Blaustein, R. (2015). "Unraveling the Mysteries of Animal Domestication". BioScience. 65: 7–13. doi:10.1093/biosci/biu201.
^Choi, Jae; et al. (2017). "The Rice Paradox: Multiple Origins but Single Domestication in Asian Rice". Molecular Biology and Evolution. 34 (4): 969–979. doi:10.1093/molbev/msx049. PMC5400379. PMID 28087768.
^Wills, Christopher (2011). Genetic and Phenotypic Consequences of Introgression Between Humans and Neanderthals. Advances in Genetics. Vol. 76. pp. 27–54. doi:10.1016/B978-0-12-386481-9.00002-X. ISBN9780123864819. PMID 22099691.
^Review of scientific papers on gene introgression between wild and domestic cats
^Review and link to scientific papers regarding introgression of dog genes into wild canid populations
^Arnold, M. L. & Bennett, B. D. (1993). Natural Hybridization in Louisiana irises: genetic variation and ecological determinants. In: Harrison, R. G. ed. (1993). Hybrid Zones and Evolutionary Process, pp. 115–139. New York: Oxford University Press. ISBN978-0-19-506917-4
^Arnold, Michael L. (1994). "Natural Hybridization and Louisiana Irises". BioScience. 44 (3): 141–147. doi:10.2307/1312250. ISSN 0006-3568. JSTOR 1312250.
^Espinasa, Luis; Robinson, Jenna; Soares, Daphne; Hoese, Geoffrey; Toulkeridis, Theofilos; Iii, Rickard Toomey (2018-08-15). "Troglomorphic features of Astroblepus pholeter, a cavefish from Ecuador, and possible introgressive hybridization". Subterranean Biology. 27: 17–29. doi:10.3897/subtbiol.27.27098. ISSN 1314-2615.
^Eshed, Y (1995) An Introgression Line Population of Lycopersicon pennellii in the Cultivated Tomato Enables the Identification and Fine Mapping of Yield-Associated QTL
^Garrick, Ryan C.; Banusiewicz, John D.; Burgess, Stephanie; Hyseni, Chaz; Symula, Rebecca E. (2019). "Extending phylogeography to account for lineage fusion". Journal of Biogeography. 46 (2): 268–278. doi:10.1111/jbi.13503. S2CID 91682713.
^Garrick, Ryan C.; Benavides, Edgar; Russello, Michael A.; Hyseni, Chaz; Edwards, Danielle L.; Gibbs, James P.; Tapia, Washington; Ciofi, Claudio; Caccone, Adalgisa (2014). "Lineage fusion in Galápagos giant tortoises". Molecular Ecology. 23 (21): 5276–5290. doi:10.1111/mec.12919. PMID 25223395. S2CID 36180329.
Further reading
Arnold, M. L. (2007). Evolution through Genetic Exchange. New York: Oxford University Press. ISBN978-0-19-922903-1.
Anderson, E. (1949). Introgressive Hybridization. New York: Wiley.
Eyal Friedman; et al. (2004). "Zooming In on a Quantitative Trait for Tomato Yield Using Interspecific Introgressions". Science. 305 (5691): 1786–1798. Bibcode:2004Sci...305.1786F. doi:10.1126/science.1101666. PMID 15375271. S2CID 24142071.
Rieseberg, L. H.; Wendel, J. F. (1993). "Introgression and its consequences in plants". In Harrison, R. G. (ed.). Hybrid Zones and Evolutionary Process. New York: Oxford University Press. pp. 70–109. ISBN978-0-19-506917-4.
Martinsen G. D.; Whitham R. J. Turek; Keim P. (2001). "Hybrid populations selectively filter gene introgression between species". Evolution. 55 (7): 1325–1335. doi:10.1554/0014-3820(2001)055[1325:hpsfgi]2.0.co;2. PMID 11525457.
Whitney, K.D., Ahern J.R.,Campbell L.G, Albert L.P., King M.S. (2010). "Patterns of hybridization in plants" (PDF). Perspectives in Plant Ecology, Evolution and Systematics. 12 (3): 175–182. doi:10.1016/j.ppees.2010.02.002.{{cite journal}}: CS1 maint: multiple names: authors list (link) ("Forbidden" - No Access 2015-04-06) Alternate Link:
January 20, 2023
introgression, also, known, introgressive, hybridization, genetics, transfer, genetic, material, from, species, into, gene, pool, another, repeated, backcrossing, interspecific, hybrid, with, parent, species, long, term, process, even, when, artificial, take, . Introgression also known as introgressive hybridization in genetics is the transfer of genetic material from one species into the gene pool of another by the repeated backcrossing of an interspecific hybrid with one of its parent species Introgression is a long term process even when artificial it may take many hybrid generations before significant backcrossing occurs This process is distinct from most forms of gene flow in that it occurs between two populations of different species rather than two populations of the same species A phylogenetic model of introgressive hybridization the hybrid zone of the two species lineages is shown in blue with each horizontal line representing an individual introgressive event Introgression also differs from simple hybridization Simple hybridization results in a relatively even mixture gene and allele frequencies in the first generation will be a uniform mix of two parental species such as that observed in mules Introgression on the other hand results in a complex highly variable mixture of genes and may only involve a minimal percentage of the donor genome Contents 1 Definition 2 Source of variation 3 Examples 3 1 Humans 3 2 Birds 3 3 Butterflies 3 4 Domestic species 3 5 Plants 3 6 Fish 4 Introgression line 5 Lineage fusion 6 See also 7 References 8 Further readingDefinition EditIntrogression or introgressive hybridization is the incorporation usually via hybridization and backcrossing of novel genes and or alleles from one taxon into the gene pool of a second distinct taxon 1 2 3 4 This introgression is considered adaptive if the genetic transfer results in an overall increase in the recipient taxon s fitness 5 Ancient introgression events can leave traces of extinct species in present day genomes a phenomenon known as ghost introgression 6 Source of variation EditIntrogression is an important source of genetic variation in natural populations and may contribute to adaptation and even adaptive radiation 7 It can occur across hybrid zones due to chance selection or hybrid zone movement 8 There is evidence that introgression is a ubiquitous phenomenon in plants and animals 9 10 including humans 11 in which it may have introduced the microcephalin D allele 12 It has been proposed that historically introgression with wild animals is a large contributor to the wide range of diversity found in domestic animals rather than multiple independent domestication events 13 Introgressive hybridization has also been shown to be important in the evolution of domesticated crop species possibly providing genes that help in their expansion into different environments A genomic study from New York University Abu Dhabi Center for Genomics and Systems Biology showed that domesticated date palm varieties from North Africa show introgressive hybridization of between 5 18 of its genome from the wild Cretan palm Phoenix theophrasti into Middle East date palms P dactylifera This process is also similar to the evolution of apples by hybridization of Central Asian apples with the European crabapple 14 It has also been shown that indica rice arose when Chinese japonica rice arrived in India about 4 500 years ago and hybridized with an undomesticated proto indica or wild O nivara and transferred key domestication genes from japonica to indica 15 Examples EditHumans Edit Main article Interbreeding between archaic and modern humans There is strong evidence for the introgression of Neanderthal genes 16 and Denisovan genes 17 into parts of the modern human gene pool Birds Edit The Mallard duck is possibly the world s most capable bird to hybridise with other duck species often to the point of the loss of genetic identity of these species For example feral mallard populations have significantly reduced wild populations of the Pacific black duck in New Zealand and Australia through cross breeding citation needed Butterflies Edit One important example of introgression has been observed in studies of mimicry in the butterfly genus Heliconius 18 This genus includes 43 species and many races with different color patterns Congeners exhibiting overlapping distributions show similar color patterns The subspecies H melpomene amaryllis and H melpomene timareta ssp nov overlap in distribution Using the ABBA BABA test some researchers have observed that there is about 2 to 5 introgression between the pair of subspecies Importantly the introgression is not random The researchers saw significant introgression in chromosomes 15 and 18 where important mimicry loci are found loci B D and N Yb They compared both subspecies with H melpomene agalope which is a subspecies near H melpomene amaryllis in entire genome trees The result of the analysis was that there is no relation between those two species and H melpomene agalope in the loci B D and N Yb Moreover they performed the same analysis with two other species with overlapping distributions H timareta florencia and H melpomene agalope They demonstrated introgression between the two taxa especially in the loci B D and N Yb Finally they concluded their experiments with sliding window phylogenetic analyses estimating different phylogenetic trees depending on the different regions of the loci When a locus is important in the color pattern expression there is a close phylogenetic relationship between the species When the locus is not important in the color pattern expression the two species are phylogenetically distant because there is no introgression at such loci Domestic species Edit Introgression can have a significant impact on non human populations through hybridization for instance between wild and domestic populations of animals This includes household pets as seen in cats 19 or in dogs 20 Plants Edit Main article Introgressive hybridization in plants Introgression has been observed in several plant species For instance a species of iris from southern Louisiana has been studied by Arnold amp Bennett 1993 regarding the increased fitness of hybrid variants 21 22 Fish Edit Espinasa et al found that introgression between a surface dwelling members of Astroblepus and a troglomorphic species Astroblepus pholeter resulted in the development of previously lost traits in offspring such as distinct eyes and optic nerves 23 Introgression line EditAn introgression line IL is a crop species that contains genetic material artificially derived from a wild relative population through repeated backcrossing An example of a collection of ILs called an IL Library is the use of chromosome segments from Solanum pennellii a wild species of tomato that was introgressed into Solanum lycopersicum the cultivated tomato The lines of an IL library usually cover the complete genome of the donor Introgression lines allow the study of quantitative trait loci but also the creation of new varieties by introducing exotic traits 24 Lineage fusion Edit Lineage fusion on a phylogenetic tree individual introgression events within the hybrid zone blue are shown as horizontal lines Hybrids are produced before the lineages fuse but rejoin one of the two lineages Neither species A nor B remains extant in the area of interest Lineage fusion is an extreme variant of introgression that results from the merging of two distinct species or populations This eventually results in a single population that displaces or replaces the parental species in the region 25 Some lineage fusion occurs soon after two taxa diverge or speciate especially if there are few reproductive barriers between lineages 26 It is not strictly necessary for the two lineages to be closely related but rather have the ability to produce viable offspring See also EditChimera genetics Genetic engineering Genetic erosion Genetic pollution Transgene Transgenic plantReferences Edit Anderson Edgar Hubricht Leslie 1938 Hybridization in Tradescantia III The Evidence for Introgressive Hybridization American Journal of Botany 25 6 396 doi 10 2307 2436413 JSTOR 2436413 Anderson E 1949 Introgressive hybridization New York Wiley amp Sons Harrison R 2014 Hybridization Introgression and the Nature of Species Boundaries Journal of Heredity 105 795 809 doi 10 1093 jhered esu033 PMID 25149255 Ottenburghs Jente Kraus Robert H S van Hooft Pim van Wieren Sipke E Ydenberg Ronald C Prins Herbert H T 2017 Avian introgression in the genomic era Avian Research 8 1 30 doi 10 1186 s40657 017 0088 z ISSN 2053 7166 Suarez Gonzalez Adriana Lexer Christian Cronk Quentin C B 2018 03 31 Adaptive introgression a plant perspective Biology Letters 14 3 20170688 doi 10 1098 rsbl 2017 0688 PMC 5897607 PMID 29540564 Jente Ottenburghs 2020 Ghost Introgression Spooky Gene Flow in the Distant Past BioEssays https doi org 10 1002 bies 202000012 Grant P R Grant B R Petren K 2005 Hybridization in the Recent Past The American Naturalist 166 1 56 67 doi 10 1086 430331 PMID 15937789 S2CID 23841467 a href Template Cite journal html title Template Cite journal cite journal a CS1 maint multiple names authors list link Richard Buggs 2007 Empirical study of hybrid zone movement Heredity 99 3 301 312 doi 10 1038 sj hdy 6800997 PMID 17611495 Dowling T E Secor C L 1997 The role of hybridization and introgression in the diversification of animals Annual Review of Ecology and Systematics 28 593 619 doi 10 1146 annurev ecolsys 28 1 593 S2CID 52367016 Bullini L 1994 Origin and evolution of animal hybrid species Trends in Ecology and Evolution 9 11 422 426 doi 10 1016 0169 5347 94 90124 4 PMID 21236911 Holliday T W 2003 Species concepts reticulations and human evolution Current Anthropology 44 5 653 673 doi 10 1086 377663 S2CID 85569586 Evans Pd Mekel Bobrov N Vallender Ej Hudson Rr Lahn Bt Nov 2006 Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage Proceedings of the National Academy of Sciences of the United States of America 103 48 18178 83 Bibcode 2006PNAS 10318178E doi 10 1073 pnas 0606966103 ISSN 0027 8424 PMC 1635020 PMID 17090677 Blaustein R 2015 Unraveling the Mysteries of Animal Domestication BioScience 65 7 13 doi 10 1093 biosci biu201 Flowers Jonathan et al 2019 Cross species hybridization and the origin of North African date palms Proceedings of the National Academy of Sciences USA 116 5 1651 1658 doi 10 1073 pnas 1817453116 PMC 6358688 PMID 30642962 Choi Jae et al 2017 The Rice Paradox Multiple Origins but Single Domestication in Asian Rice Molecular Biology and Evolution 34 4 969 979 doi 10 1093 molbev msx049 PMC 5400379 PMID 28087768 Wills Christopher 2011 Genetic and Phenotypic Consequences of Introgression Between Humans and Neanderthals Advances in Genetics Vol 76 pp 27 54 doi 10 1016 B978 0 12 386481 9 00002 X ISBN 9780123864819 PMID 22099691 Huerta Sanchez Emilia Jin Xin Asan Bianba Zhuoma Peter Benjamin M Vinckenbosch Nicolas Liang Yu Yi Xin He Mingze Somel Mehmet Ni Peixiang Wang Bo Ou Xiaohua Huasang Luosang Jiangbai Cuo Zha Xi Ping Li Kui Gao Guoyi Yin Ye Wang Wei Zhang Xiuqing Xu Xun Yang Huanming Li Yingrui Wang Jian Wang Jun Nielsen Rasmus 2014 Altitude adaptation in Tibetans caused by introgression of Denisovan like DNA Nature 512 7513 194 197 Bibcode 2014Natur 512 194H doi 10 1038 nature13408 PMC 4134395 PMID 25043035 The Heliconius Genome Consortium 2012 Butterfly genome reveals promiscuous exchange of mimicry adaptations among species Nature 487 7405 94 98 Bibcode 2012Natur 487 94T doi 10 1038 nature11041 PMC 3398145 PMID 22722851 Review of scientific papers on gene introgression between wild and domestic cats Review and link to scientific papers regarding introgression of dog genes into wild canid populations Arnold M L amp Bennett B D 1993 Natural Hybridization in Louisiana irises genetic variation and ecological determinants In Harrison R G ed 1993 Hybrid Zones and Evolutionary Process pp 115 139 New York Oxford University Press ISBN 978 0 19 506917 4 Arnold Michael L 1994 Natural Hybridization and Louisiana Irises BioScience 44 3 141 147 doi 10 2307 1312250 ISSN 0006 3568 JSTOR 1312250 Espinasa Luis Robinson Jenna Soares Daphne Hoese Geoffrey Toulkeridis Theofilos Iii Rickard Toomey 2018 08 15 Troglomorphic features of Astroblepus pholeter a cavefish from Ecuador and possible introgressive hybridization Subterranean Biology 27 17 29 doi 10 3897 subtbiol 27 27098 ISSN 1314 2615 Eshed Y 1995 An Introgression Line Population of Lycopersicon pennellii in the Cultivated Tomato Enables the Identification and Fine Mapping of Yield Associated QTL Garrick Ryan C Banusiewicz John D Burgess Stephanie Hyseni Chaz Symula Rebecca E 2019 Extending phylogeography to account for lineage fusion Journal of Biogeography 46 2 268 278 doi 10 1111 jbi 13503 S2CID 91682713 Garrick Ryan C Benavides Edgar Russello Michael A Hyseni Chaz Edwards Danielle L Gibbs James P Tapia Washington Ciofi Claudio Caccone Adalgisa 2014 Lineage fusion in Galapagos giant tortoises Molecular Ecology 23 21 5276 5290 doi 10 1111 mec 12919 PMID 25223395 S2CID 36180329 Further reading EditArnold M L 2007 Evolution through Genetic Exchange New York Oxford University Press ISBN 978 0 19 922903 1 Anderson E 1949 Introgressive Hybridization New York Wiley Decobert O 2017 Complement a l inventaire des Carabini du Midi toulousain Coleoptera Carabidae Carnets natures 2017 vol 4 33 38 ISSN 2427 6111 https carnetsnatures fr volume4 carabidae decobert pdf Eyal Friedman et al 2004 Zooming In on a Quantitative Trait for Tomato Yield Using Interspecific Introgressions Science 305 5691 1786 1798 Bibcode 2004Sci 305 1786F doi 10 1126 science 1101666 PMID 15375271 S2CID 24142071 Rieseberg L H Wendel J F 1993 Introgression and its consequences in plants In Harrison R G ed Hybrid Zones and Evolutionary Process New York Oxford University Press pp 70 109 ISBN 978 0 19 506917 4 Martinsen G D Whitham R J Turek Keim P 2001 Hybrid populations selectively filter gene introgression between species Evolution 55 7 1325 1335 doi 10 1554 0014 3820 2001 055 1325 hpsfgi 2 0 co 2 PMID 11525457 Whitney K D Ahern J R Campbell L G Albert L P King M S 2010 Patterns of hybridization in plants PDF Perspectives in Plant Ecology Evolution and Systematics 12 3 175 182 doi 10 1016 j ppees 2010 02 002 a href Template Cite journal html title Template Cite journal cite journal a CS1 maint multiple names authors list link Forbidden No Access 2015 04 06 Alternate Link Patterns of Hybridization in Plants Retrieved from https en wikipedia org w index php title Introgression amp oldid 1131259827, wikipedia, wiki, book, books, library,
