Impacts of natural hybridization and introgression on biological invasion of plant species

doi:10.3724/SP.J.2010.577

Abstract

Abstract:

Biological invasions have caused tremendous ecological and socio-economic damages worldwide. Therefore, it is important to develop methods for their effective management. Biological invasion is a process of adaptive evolution in which hybridization and introgression play an important role in promoting invasive species by changing their invasiveness. Therefore, understanding how the genetic mechanisms of hybridization and introgression influence biological invasion will facilitate effective control of invasive species. The escape of transgenes with special functions into populations of wild relatives through hybridization and introgression may change the invasiveness and weediness of the wild relatives, causing undesired environmental problems. This paper introduces the role of hybridization and introgression in adaptive evolution and speciation, and discusses how an alien species can change its adaptability, competitive ability, and invasiveness in new habitats through introgressive hybridization. Hybridization and introgression can cause polyploid and homoploid evolution of plant species, thereby influencing the fitness of new species and promoting the formation of an invasive species in new habitats. At the same time, with the rapid development of transgenic technologies, transgenic crops are being extensively released into the environment for commercial production. Biological invasion is a complicated evolutionary and ecological process, and future research should investigate the roles of hybridization and introgression in biological invasions in the context of the myriad factors that influence the process.

Key words: biological invasion, introgressive hybridization, fitness, ecological safety, adaptive evolution, polyploid, homoploid

Bao-Rong Lu, Hui Xia, Wei Wang, Xiao Yang. Impacts of natural hybridization and introgression on biological invasion of plant species[J]. Biodiv Sci, 2010, 18(6): 577-589.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.3724/SP.J.2010.577

https://www.biodiversity-science.net/EN/Y2010/V18/I6/577

Figures/Tables 2

Fig. 1 A schematic illustration demonstrates allopolyploid and homoploid speciation that can significantly promote genetic variation and invasiveness of the newly formed species. (1) A tetraploid species evolved through the natural hybridization of two diploid species with different genomes (AA or BB) followed by chromosome doubling. The newly formed tetraploid species contains the AABB genomes from both parents and may have a much larger body size and more abundant genetic recombinants than its diploid parents. (2) A homoploid species evolved through the natural hybridization of two closely related diploid species with the same AA genome. The newly formed diploid species contains the AA genome without any change in chromosome numbers and is partially or fully fertile with new genetic recombinants from the two parents.

Fig. 2 A schematic illustration demonstrates introgressive hybridization between individuals of the same or closely related or species to promote genetic variation and invasiveness. Through the hybridization-introgression process: crosses between two individuals and backcrosses of the hybrids with both parents, a large number of new genetic recombinants are generated in hybrid populations and their offspring. Plants 1, 5 represent the parental types, plants 2, 3, 4 represents a wide range of recombination and segregation types, including the “super type” (plant 4) from transgressive segregation.

References 94

[1]	Abbott RJ, Brennan AC, James JK, Forbes DG, Hegarty MJ, Hiscock SJ (2009) Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort ( Senecio squalidus L., Asteraceae). Biological Invasions, 11, 1145-1158.
[2]	Ainouche ML, Baumel A, Salmon A, Yannic G (2004) Hybridization, polyploidy and speciation in Spartina Schreb. (Poaceae). New Phytologist, 161, 165-172.
[3]	Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biological Invasions, 11, 1159-1173.
[4]	Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conservation Biology, 17, 24-30.
[5]	Alpert P (2006) The advantages and disadvantages of being introduced. Biological Invasions, 8, 1523-1534.
[6]	Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecology Letters, 9, 196-214. URL PMID
[7]	Baack EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Current Opinion in Genetics and Development, 17, 513-518. DOI URL PMID
[8]	Baack EJ, Whitney KD, Rieseberg LH (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytologist, 167, 623-630.
[9]	Barrett SCH (1983) Crop mimicry in weeds. Economic Botany, 37, 25-28.
[10]	Bartomeus I, Vilá M, Steffan-Dewenter I (2010) Combined effects of Impatiens glandulifera invasion and landscape structure on native plant pollination. Journal of Ecology, 98, 440-450.
[11]	Bartsch D, Brand U, Morak C, Pohl-Orf M, Schuphan I, Ellstrand NC (2001) Biosafety of hybrids between transgenic virus-resistant sugar beet and Swiss chard. Ecological Applications, 11, 142-147.
[12]	Blair AC, Hufbauer RA (2010) Hybridization and invasion: one of North America’s most devastating invasive plants shows evidence for a history of interspecific hybridization. Evolutionary Applications, 3, 40-51. DOI URL PMID
[13]	Bleeker W (2003) Hybridization and Rorippa austriaca (Brassicaceae) invasion in Germany. Molecular Ecology, 12, 1831-1841. URL PMID
[14]	Bradley BA (2010) Assessing ecosystem threats from global and regional change: hierarchical modeling of risk to sagebrush ecosystems from climate change, land use and invasive species in Nevada, USA. Ecography, 33, 198-208.
[15]	Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ (1997) Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Molecular Biology and Evolution, 14, 81-90. DOI URL PMID
[16]	Campbell LG, Snow AA, Ridley CE (2006) Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment. Ecology Letters, 9, 1198-1209. DOI URL PMID
[17]	Campbell LG, Snow AA, Sweeney PM, Ketner JM (2009) Rapid evolution in crop-weed hybrids under artificial selection for divergent life histories. Evolutionary Applications, 2, 172-186. DOI URL PMID
[18]	Cao QJ, Xia H, Yang X, Lu B-R (2009) Performance of hybrids between weedy rice and insect-resistant transgenic rice under field experiments: implication for environmental biosafety assessment. Journal of Integrative Plant Biology, 51, 1138-1148. DOI URL PMID
[19]	Chen ZY (陈中义), Li B (李博), Chen JK (陈家宽) (2004) Ecological consequences and management of Spartina spp. invasions in coastal ecosystem. Biodiversity Science (生物多样性), 12, 280-289. (in Chinese with English abstract)
[20]	Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y, Byers B (2000) Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell, 12, 1551-1567. DOI URL PMID
[21]	Culley TM, Hardiman NA (2009) The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biological Invasions, 11, 1107-1119.
[22]	Cummings CL, Alexander HM, Snow AA, Rieseberg LH, Kim MJ, Culley TM (2002) Fecundity selection in a sunflower crop-wild study: can ecological data predict crop allele changes. Ecological Applications, 12, 1661-1671.
[23]	Elam DR, Ridley CE, Goodell K, Ellstrand NC (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. Proceedings of the National Academy of Sciences, USA, 104, 549-552.
[24]	Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology and Systematics, 30, 539-563.
[25]	Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences, USA, 97, 7043-7050.
[26]	Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. Journal of Evolutionary Biology, 18, 524-535. URL PMID
[27]	Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat—a revolutionary reprogramming followed by gradual changes. Journal of Genetic Genomics, 36, 511-518.
[28]	Gressel J (2000) Molecular biology of weed control. Transgenic Research, 9, 355-382. DOI URL PMID
[29]	Hails RS, Morley K (2005) Genes invading new populations: a risk assessment perspective. Trends in Ecology and Evolution, 20, 245-252. DOI URL PMID
[30]	Hall L, Topinka K, Huffman J, Davis L, Good A (2000) Pollen flow between herbicide-resistant Brassica napus is the cause of multiple-resistant B. napus volunteers. Weed Science, 48, 688-694.
[31]	Hegarty MJ, Barker GL, Brennan AC, Edwards KJ, Abbott RJ, Hiscock SJ (2009) Extreme changes to gene expression associated with homoploid hybrid speciation. Molecular Ecology, 18, 877-889. DOI URL PMID
[32]	Hegarty MJ, Hiscock SJ (2005) Hybrid speciation in plants: new insights from molecular studies. New Phytologist, 165, 411-423.
[33]	Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biological Conservation, 89, 143-152.
[34]	Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution, 60, 1585-1595. URL PMID
[35]	Koenig WD, Ashley MV (2003) Is pollen limited? The answer is blowing in the wind. Trends in Ecology and Evolution, 18, 157-159.
[36]	Lande R (1995) Mutation and conservation. Conservation Biology, 9, 782-791.
[37]	Latta RG, Gardner KM, Johansen-Morris AD (2007) Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata. Genetica, 129, 167-177. URL PMID
[38]	Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences, USA, 104, 3883-3888.
[39]	Leger EA, Espeland EK, Merrill KR, Meyer SE (2009) Genetic variation and local adaptation at a cheatgrass (Bromus tectorum) invasion edge in western Nevada. Molecular Ecology, 18, 4366-4379. DOI URL PMID
[40]	Lexer C, Welch ME, Durphy JL, Rieseberg LH (2003) Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology, 12, 1225-1235. URL PMID
[41]	Londo LP, Schaal BA (2007) Origins and population genetics of weedy red rice in the USA. Molecular Ecology, 16, 4523-4535. URL PMID
[42]	Lowe AJ, Abbott RJ (2000) Routes of origin of two recently evolved hybrid taxa: Senecio vulgaris var. hibernicus and York radiate groundsel (Asteraceae). American Journal of Botany, 87, 1159-1167. URL PMID
[43]	Lu B-R, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. BioScience, 55, 669-678.
[44]	Lu B-R, Yang C (2009) Gene flow from genetically modified rice to its wild relatives: assessing potential ecological consequences. Biotechnology Advances, 27, 1083-1091. DOI URL PMID
[45]	Mack RH, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications, 10, 689-710.
[46]	Mallet J (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229-237. DOI URL PMID
[47]	Milne RI, Abbott RJ (2000) Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British Isles. Molecular Ecology, 9, 541-556. DOI URL PMID
[48]	Moon HS, Li Y, Stewart CN Jr (2009) Keeping the genie in the bottle: transgene biocontainment by excision in pollen. Trends in Biotechnology, 28, 3-8. URL PMID
[49]	NRCNA (National Research Council of the National Academies) (2004) Biological Confinement of Genetically Engineered Organisms. The National Academies Press, Washington D. C., USA.
[50]	Olson A, Paul J, Freeland JR (2009) Habitat preferences of cattail species and hybrids ( Typha spp.) in eastern Canada. Aquatic Botany, 91, 67-70.
[51]	Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien MA (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytologist, 186, 37-45.
[52]	Pearson DE (2009) Invasive plant architecture alters trophic interactions by changing predator abundance and behavior. Oecologia, 159, 549-558. URL PMID
[53]	Peltzer DA, Allen RB, Lovett GM, Whitehead D, Wardle DA (2010) Effects of biological invasions on forest carbon sequestration. Global Change Biology, 16, 732-746.
[54]	Pétillon J, Puzin C, Acou A, Outreman Y (2009) Plant invasion phenomenon enhances reproduction performance in an endangered spider. Aturwissenschaften, 96, 1241-1246.
[55]	Petit RJ (2004) Biological invasions at the gene level. Diversity and Distributions, 10, 159-165.
[56]	Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52, 273-288.
[57]	Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends in Plant Science, 13, 288-294. URL PMID
[58]	Prevéy JS, Germino MJ, Huntly NJ, Inouye RS (2010) Exotic plants increase and native plants decrease with loss of foundation species in sagebrush steppe. Plant Ecology, 207, 39-51.
[59]	Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Biological Invasions (ed. Nentwig W), pp. 97- 125. Springer, New York.
[60]	Rejmănek M (2000) Invasive plants: approaches and predictions. Austral Ecology, 25, 497-506.
[61]	Ridley CE, Ellstrand NC (2009) Rapid evolution of morphology and adaptive life history in the invasive California wild radish ( Raphanus sativus) and the implications for management. Evolutionary Applications, 3, 64-76. DOI URL PMID
[62]	Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity, 83, 363-372. URL PMID
[63]	Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytologist, 140, 599-624.
[64]	Rieseberg LH, Kim SC, Randell RA, Whitney KD, Gross BL, Lexer C, Clay K (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica, 129, 149-165. URL PMID
[65]	Rieseberg LH, Sinervo B, Linder CR, Ungerer MC, Arias DM (1996) Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science, 272, 741-745. DOI URL PMID
[66]	Rieseberg LH, Sternberg SB, Doan K (1990) Helianthus annuus ssp. texanus has chloroplast DNA and unclear ribosomal RNA genes of Helianthus deblilis ssp. cucumerifolius. Proceedings of the National Academy of Sciences, USA, 87, 593-597. DOI URL
[67]	Rieseberg LH, Widmer A, Arntz AM, Burke B (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philosophical Transactions of the Royal Society B: Biological Sciences, 358, 1141-1147. DOI URL
[68]	Rosenthal DM, Schwarzbach AE, Donovan LA, Raymond O, Rieseberg LH (2002) Phenotypic differentiation between three ancient hybrid taxa and their parental species. International Journal of Plant Science, 163, 387-398. DOI URL
[69]	Rout ME, Chrzanowski TH (2009) The invasive Sorghum halepense harbors endophytic N₂-fixing bacteria and alters soil biogeochemistry. Plant and Soil, 315, 163-172. DOI URL
[70]	Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. Journal of Ecology, 97, 247-255. DOI URL
[71]	Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Biological Invasions, 11, 1093-1105. DOI URL
[72]	Schweitzer JA, Martinsen GD, Whitham TG (2002) Cottonwood hybrids gain fitness traits of both parents: a mechanism for their long-term persistence? American Journal of Botany, 89, 981-991. URL PMID
[73]	Snow AA, Pilson D, Rieseberg LH, Paulsen MJ, Pleskac N, Reagon MR, Wolf DE, Selbo SM (2003) A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecological Applications, 13, 279-286. DOI URL
[74]	Stebbins GL (1959) The role of hybridization in evolution. Proceedings of the American Philosophical Society, 103, 231-251.
[75]	Stewart NC, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Reviews Genetics, 4, 806-817. DOI URL PMID
[76]	Sun JX (孙静贤), Ding KY (丁开宇), Wang BY (王兵益) (2005) The review and prospect of plant polyploid research. Journal of Wuhan Botanical Research, 23, 482-490.
[77]	Sun XY, Lu ZH, Sang WG (2004) Review on studies of Eupatorium adenophorum—an important invasive species in China. Journal of Forestry Research, 15, 319-322. DOI URL
[78]	Takakura KI, Nishida T, Matsumoto T, Nishida S (2009) Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects. Biological Invasions, 11, 973-981. DOI URL
[79]	Travis SE, Marburger JE, Windels S, Kubátova B (2010) Hybridization dynamics of invasive cattail (Typhaceae) stands in the Western Great Lakes Region of North America: a molecular analysis. Journal of Ecology, 98, 7-16. DOI URL
[80]	Ungerer MC, Baird SJE, Pan J, Rieseberg LH (1998) Rapid hybrid speciation in wild sunflowers. Proceedings of the National Academy of Sciences, USA, 95, 11757-11762. DOI URL
[81]	Urbanska KM, Hurka H, Landolt E, Neuffer B, Mummenhoff K (1997) Hybridization and evolution in Cardamine L. (Brassicaceae) at Urnerboden, Central Switzerland: biosystematic and molecular evidence. Plant Systematics and Evolution, 204, 233-256. DOI URL
[82]	Vacher C, Weis AE, Hermann D, Kossler T, Young C, Hochberg ME (2004) Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa). Theoretical and Applied Genetics, 109, 806-814. DOI URL PMID
[83]	Vila M, D'Antonio CM (1998) Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecological Applications, 8, 1196-1205.
[84]	Virah-Sawmy M, Mauremootoo J, Marie D, Motala S, Seva- thian JC (2009) Rapid degradation of a Mauritian rainforest following 60 years of plant invasion. Oryx, 43, 599-607. DOI URL
[85]	von Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecology Letters, 13, 235-245. URL PMID
[86]	Wang Q (王卿), An SQ (安树青), Ma ZJ (马志军), Zhao B (赵斌), Chen JK (陈家宽), Li B (李博) (2006) Invasive Spartina alterniflora: biology, ecology and management. Acta Phytotaxonomica Sinica, 44, 559-588. DOI URL
[87]	Weinig C, Brock MT, Dechaine JA, Welch SM (2007) Resolving the genetic basis of invasiveness and predicting invasions. Genetica, 129, 205-216. URL PMID
[88]	Welch ME, Rieseberg LH (2002) Habitat divergence between a homoploid hybrid sunflower species, Helianthus paradoxus (Asteraceae), and its progenitors. American Journal of Botany, 89, 472-478. DOI URL PMID
[89]	Whitney KD, Ahern JR, Campbell LG (2009) Hybridization-prone plant families do not generate more invasive species. Biological Invasions, 11, 1205-1215. DOI URL
[90]	Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14, 569-580. DOI URL
[91]	Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. The American Naturalist, 167, 794-807. DOI URL PMID
[92]	Wolfe LM, Blair AC, Penna BM (2007) Does intraspecific hybridization contribute to the evolution of invasiveness? an experimental test. Biological Invasions, 9, 515-527. DOI URL
[93]	Xu H, Ding H, Li MY, Qiang S, Guo JY, Han ZM, Huang ZG, Sun HY, He SP, Wu HR, Wan FH (2006) The distribution and economic losses of alien species invasion to China. Biological Invasions, 8, 1495-1500. DOI URL
[94]	Zayed A, Constantin SA, Packer L (2007) Successful biological invasion despite a severe genetic load. PLoS ONE, 9, 1-6.