Introgression

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.

Introgressive phylogenetic clade
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.

Definition

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]

Examples

Humans
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

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.

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 between wild and domestic populations of animals. This includes household pets, as seen in cats[19] or in dogs.[20]

Plants
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 & 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 between two species to form a hybrid lineage.
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

References
  1. 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.
  2. Anderson E, 1949. Introgressive hybridization. New York: Wiley & Sons
  3. Harrison, R (2014). "Hybridization, Introgression, and the Nature of Species Boundaries". Journal of Heredity. 105: 795–809. doi:10.1093/jhered/esu033. PMID 25149255.
  4. 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.
  5. 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.
  6. Jente Ottenburghs (2020) Ghost Introgression: Spooky Gene Flow in the Distant Past. BioEssays. https://doi.org/10.1002/bies.202000012
  7. 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)
  8. Richard Buggs (2007). "Empirical study of hybrid zone movement". Heredity. 99 (3): 301–312. doi:10.1038/sj.hdy.6800997. PMID 17611495.
  9. 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.
  10. 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.
  11. Holliday T. W. (2003). "Species concepts, reticulations, and human evolution". Current Anthropology. 44 (5): 653–673. doi:10.1086/377663. S2CID 85569586.
  12. 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.
  13. Blaustein, R. (2015). "Unraveling the Mysteries of Animal Domestication". BioScience. 65: 7–13. doi:10.1093/biosci/biu201.
  14. 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. Bibcode:2019PNAS..116.1651F. doi:10.1073/pnas.1817453116. PMC 6358688. PMID 30642962.
  15. 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.
  16. 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.
  17. Huerta-Sánchez, 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.
  18. 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.
  19. Review of scientific papers on gene introgression between wild and domestic cats
  20. Review and link to scientific papers regarding introgression of dog genes into wild canid populations
  21. 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. ISBN 978-0-19-506917-4
  22. Arnold, Michael L. (1994). "Natural Hybridization and Louisiana Irises". BioScience. 44 (3): 141–147. doi:10.2307/1312250. ISSN 0006-3568. JSTOR 1312250.
  23. 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.
  24. Eshed, Y (1995) An Introgression Line Population of Lycopersicon pennellii in the Cultivated Tomato Enables the Identification and Fine Mapping of Yield-Associated QTL
  25. 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.
  26. 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
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