Hybridisation is associated with increased fecundity and size in invasive taxa: Meta-analytic support for the hybridisation-invasion hypothesis

Ecology Letters

Volumn 17, Issue 11, 2014, Pages 1464-1477

  Hovick, Stephen M ^a   Whitney, Kenneth D ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Adaptive evolution; Colonisation; Hybridisation; Introgression; Invasion genetics; Phylogenetic meta analysis; Polyploidy; Range expansion; Weeds

Indexed keywords

ANIMAL; FERTILITY; FUNGUS; GENETIC SELECTION; HYBRIDIZATION; INTRODUCED SPECIES; META ANALYSIS; PHYLOGENY; PLANT;

ANIMALS; FERTILITY; FUNGI; HYBRIDIZATION, GENETIC; INTRODUCED SPECIES; PHYLOGENY; PLANTS; SELECTION, GENETIC;

EID: 84907810058     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12355     Document Type: Review

References (100)

1. Abbott, R.J. (1992). Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol. Evol., 7, 401-405.
2. Albertin, W. & Marullo, P. (2012). Polyploidy in fungi: evolution after whole-genome duplication. Proc. Biol. Sci., 279, 2497-2509.
3. Anderson, E. (1948). Hybridization of the habitat. Evolution, 2, 1-9.
4. Anderson, E. & Stebbins, G.L. (1954). Hybridization as an evolutionary stimulus. Evolution, 8, 378-388.
5. Arnold, M.L. & Hodges, S.A. (1995). Are natural hybrids fit or unfit relative to their parents? Trends Ecol. Evol., 10, 67-71.
6. Arnold, M.L. & Martin, N.H. (2010). Hybrid fitness across time and habitats. Trends Ecol. Evol., 25, 530-536.
7. Arriola, P.E. & Ellstrand, N.C. (1997). Fitness of interspecific hybrids in the genus Sorghum: Persistence of crop genes in wild populations. Ecol. Appl., 7, 512-518.
8. Ayres, D.R., Smith, D.L., Zaremba, K., Klohr, S. & Strong, D.R. (2004). Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol. Invasions, 6, 221-231.
9. Ayres, D.R., Zaremba, K., Sloop, C.M. & Strong, D.R. (2008). Sexual reproduction of cordgrass hybrids (Spartina foliosa x alterniflora) invading tidal marshes in San Francisco Bay. Divers. Distrib., 14, 187-195.
10. Bailey, J. (2013). The Japanese knotweed invasion viewed as a vast unintentional hybridisation experiment. Heredity, 110, 105-110.
11. Baker, H.G. (1974). The evolution of weeds. Annu. Rev. Ecol. Syst., 5, 1-24.
12. Baker, H.G. & Stebbins, G.L. (1965). The Genetics of Colonizing Species. Academic Press New York, NY.
13. Barton, N.H. & Hewitt, G.M. (1985). Analysis of hybrid zones. Annu. Rev. Ecol. Syst., 16, 113-148.
14. te Beest, M., Le Roux, J.J., Richardson, D.M., Brysting, A.K., Suda, J., Kubesova, M. et al. (2012). The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot., 109, 19-45.
15. Blum, M.J., Walters, D.M., Burkhead, N.M., Freeman, B.J. & Porter, B.A. (2010). Reproductive isolation and the expansion of an invasive hybrid swarm. Biol. Invasions, 12, 2825-2836.
16. Brabec, J. & Pyšek, P. (2000). Establishment and survival of three invasive taxa of the genus Reynoutria (Polygonaceae) in mesic mown meadows: a field experimental study. Folia Geobotanica, 35, 27-42.
17. Brennan, A.C., Barker, D., Hiscock, S.J. & Abbott, R.J. (2012). Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae). Heredity, 108, 87-95.
18. Campbell, L.G. & Snow, A.A. (2007). Competition alters life history and increases the relative fecundity of crop-wild radish hybrids (Raphanus spp.). New Phytol., 173, 648-660.
19. Campbell, L.G., Snow, A.A. & Ridley, C.E. (2006). Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment. Ecol. Lett., 9, 1198-1209.
20. Chamberlain, S.A., Hovick, S.M., Dibble, C.J., Rasmussen, N.L., Van Allen, B.G., Maitner, B.S. et al. (2012). Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta-analysis. Ecol. Lett., 15, 627-636.
21. Crawford, K.M. & Whitney, K.D. (2010). Population genetic diversity influences colonization success. Mol. Ecol., 19, 1253-1263.
22. Culley, T.M. & Hardiman, N.A. (2009). The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biol. Invasions, 11, 1107-1119.
23. Darling, J.A., Bagley, M.J., Roman, J., Tepolt, C.K. & Geller, J.B. (2008). Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol. Ecol., 17, 4992-5007.
24. Ellstrand, N.C. & Schierenbeck, K.A. (2000). Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl Acad. Sci. USA, 97, 7043-7050.
25. Elton, C.E. (1958). The Ecology of Invasions by Animals and Plants. Methuen & Company Ltd, London, UK.
26. Flora of North America Editorial Committee (1993+).Flora of North America North of Mexico. New York and Oxford.
27. Funk, V.A., Susanna, A., Stuessey, F.T. & Bayer, R.J. (2009). Systematics, Evolution, and Biogeography of Compositae. International Association for Plant Taxonomy Vienna, Austria.
28. Gallagher, K.G., Schierenbeck, K.A. & Dantonio, C.M. (1997). Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California. 2. Allozyme evidence. Am. J. Bot., 84, 905-911.
29. Gammon, M.A., Baack, E., Orth, J.F. & Kesseli, R. (2010). Viability, Growth, and Fertility of Knotweed Cytotypes in North America. Invasive Plant Sci. Manage., 3, 208-218.
30. Geiger, J.H., Pratt, P.D., Wheeler, G.S. & Williams, D.A. (2011). Hybrid vigor for the invasive exotic Brazilian peppertree (Schinus terebinthifolius Raddi., Anacardiaceae) in Florida. Int. J. Plant Sci., 172, 655-663.
31. Giraud, T., Refregier, G., Le Gac, M., de Vienne, D.M. & Hood, M.E. (2008). Speciation in fungi. Fungal Genet. Biol., 45, 791-802.
32. Grosholz, E. (2010). Avoidance by grazers facilitates spread of an invasive hybrid plant. Ecol. Lett., 13, 145-153.
33. Hahn, M.A., Buckley, Y.M. & Muller-Scharer, H. (2012). Increased population growth rate in invasive polyploid Centaurea stoebe in a common garden. Ecol. Lett., 15, 947-954.
34. Hartman, Y., Uwimana, B., Hooftman, D.A.P., Schranz, M.E., van de Wiel, C.C.M., Smulders, M.J.M. et al. (2013). Genomic and environmental selection patterns in two distinct lettuce crop-wild hybrid crosses. Evol. Appl., 6, 569-584.
35. Hasselman, D.J., Argo, E.E., McBride, M.C., Bentzen, P., Schultz, T.F., Perez-Umphrey, A.A. et al. (2014). Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Mol. Ecol., 23, 1137-1152.
36. Hawkes, C.V., Douglas, A.E. & Fitter, A.H. (2010). Origin, local experience, and the impact of biotic interactions on native and introduced Senecio species. Biol. Invasions, 12, 113-124.
37. Hedges, S.B., Dudley, J. & Kumar, S. (2006). TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics, 22, 2971-2972.
38. Henery, M.L., Bowman, G., Mraz, P., Treier, U.A., Gex-Fabry, E., Schaffner, U. et al. (2010). Evidence for a combination of pre-adapted traits and rapid adaptive change in the invasive plant Centaurea stoebe. J. Ecol., 98, 800-813.
39. Higgins, J.P.T. & Thompson, S.G. (2002). Quantifying heterogeneity in a meta-analysis. Stat. Med., 21, 1539-1558.
40. Hooftman, D.A.P., Oostermeijer, J.G.B., Jacobs, M.M.J. & Den Nijs, H.C.M. (2005). Demographic vital rates determine the performance advantage of crop-wild hybrids in lettuce. J. Appl. Ecol., 42, 1086-1095.
41. Hooftman, D.A.P., Jong, M.J.D., Oostermeijer, J.G.B. & Den Nijs, H. (2007). Modelling the long-term consequences of crop-wild relative hybridization: a case study using four generations of hybrids. J. Appl. Ecol., 44, 1035-1045.
42. Hovick, S.M., Campbell, L.G., Snow, A.A. & Whitney, K.D. (2012). Hybridization Alters Early Life-History Traits and Increases Plant Colonization Success in a Novel Region. Am. Naturalist, 179, 192-203.
43. Inderbitzin, P., Davis, R.M., Bostock, R.M. & Subbarao, K.V. (2011). The Ascomycete Verticillium longisporum Is a Hybrid and a Plant Pathogen with an Expanded Host Range. PLoS ONE, 6(3), e18260
44. Johnson, J.R., Fitzpatrick, B.M. & Shaffer, H.B. (2010). Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders. BMC Evol. Biol., 10, 147.
45. Kim, S.T., Sultan, S.E. & Donoghue, M.J. (2008). Allopolyploid speciation in Persicaria (Polygonaceae): insights from a low-copy nuclear region. Proc. Natl Acad. Sci. USA, 105, 12370-12375.
46. Kirk, H., Connolly, C. & Freeland, J.R. (2011). Molecular genetic data reveal hybridization between Typha angustifolia and Typha latifolia across a broad spatial scale in eastern North America. Aquat. Bot., 95, 189-193.
47. Lajeunesse, M.J. (2009). Meta-Analysis and the Comparative Phylogenetic Method. Am. Naturalist, 174, 369-381.
48. Lajeunesse, M.J. (2011). phyloMeta: a program for phylogenetic comparative analyses with meta-analysis. Bioinformatics, 27, 2603-2604.
49. LaRue, E.A., Grimm, D. & Thum, R.A. (2013). Laboratory crosses and genetic analysis of natural populations demonstrate sexual viability of invasive hybrid watermilfoils (Myriophyllum spicatum x M. sibiricum). Aquat. Bot., 109, 49-53.
50. Lavergne, S. & Molofsky, J. (2007). Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc. Natl Acad. Sci. USA, 104, 3883-3888.
51. Le Roux, J. & Wieczorek, A.M. (2009). Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann. Appl. Biol., 154, 1-17.
52. Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gotzsche, P.C., Ioannidis, J.P.A. et al. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. Bmj-British Medical Journal, 339, b2700.
53. Mack, R.N. (1996). Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biol. Conserv., 78, 107-121.
54. Maddison, D.R. & Schulz, K.-S. (2007). The Tree of Life Web Project. http://tolweb.org.
55. Mengersen, K., Jennions, M.D. & Schmid, C.H. (2013). Statistical models for the meta-analysis of nonindependent data. In: Handbook of Meta-Analysis in Ecology and Evolution (eds Koricheva, J., Gurevitch, J., Mengersen, K.). Princeton University Press, Princeton, NJ, pp. 255-283.
56. Moody, M.L. & Les, D.H. (2002). Evidence of hybridity in invasive watermilfoil (Myriophyllum) populations. Proc. Natl Acad. Sci. USA, 99, 14867-14871.
57. Mraz, P., Garcia-Jacas, N., Gex-Fabry, E., Susanna, A., Barres, L. & Muller-Scharer, H. (2012). Allopolyploid origin of highly invasive Centaurea stoebe s.l. (Asteraceae). Mol. Phylogenet. Evol., 62, 612-623.
58. Nechwatal, J. & Mendgen, K. (2009). Evidence for the occurrence of natural hybridization in reed-associated Pythium species. Plant. Pathol., 58, 261-270.
59. Newcombe, G., Stirling, B., McDonald, S. & Bradshaw, H.D. (2000). Melampsora xcolumbiana, a natural hybrid of M-medusae and M-occidentalis. Mycol. Res., 104, 261-274.
60. Newcombe, G., Stirling, B. & Bradshaw, H.D. (2001). Abundant pathogenic variation in the new hybrid rust Melampsora xcolumbiana on hybrid poplar. Phytopathology, 91, 981-985.
61. Pandit, M.K., Pocock, M.J.O. & Kunin, W.E. (2011). Ploidy influences rarity and invasiveness in plants. J. Ecol., 99, 1108-1115.
62. Parepa, M., Fischer, M., Krebs, C. & Bossdorf, O. (2014). Hybridization increases invasive knotweed success. Evol. Appl., 7, 413-420.
63. Perrins, J., Williamson, M. & Fitter, A. (1992). Do annual weeds have predictable characters? Acta Oecol.-Int. J. Ecol., 13, 517-533.
64. Poulsen, J.R., Osenberg, C.W., Clark, C.J., Levey, D.J. & Bolker, B.M. (2007). Plants as reef fish: fitting the functional form of seedling recruitment. Am. Naturalist, 170, 167-183.
65. Pyšek, P. & Richardson, D.M. (2007). Traits associated with invasiveness in alien plants: where do we stand? In: Biological Invasions. (ed Nentwig, W.). Springer-Verlag Berlin, Germany, pp. 97-125.
66. Pyšek, P., Brock, J.H., Bimova, K., Mandak, B., Jarosik, V., Koukolikova, I. et al. (2003). Vegetative regeneration in invasive Reynoutria (Polygonaceae) taxa: the determinant of invasibility at the genotype level. Am. J. Bot., 90, 1487-1495.
67. R Development Core Team (2013). R: A Language and Environment for Statistical Computing. (ed. R Foundation for Statistical Computing) Vienna, Austria.
68. Reagon, M., Thurber, C.S., Olsen, K.M., Jia, Y.L. & Caicedo, A.L. (2011). The long and the short of it: SD1 polymorphism and the evolution of growth trait divergence in U.S. weedy rice. Mol. Ecol., 20, 3743-3756.
69. Rejmánek, M., Richardson, D.M. & Pyšek, P. (2005). Plant invasions and invasibility of plant communities. In: Vegetation Ecology. (ed van der Maarel, E.). Blackwell, Oxford, pp. 332-355.
70. Richards, C.L., Walls, R.L., Bailey, J.P., Parameswaran, R., George, T. & Pigliucci, M. (2008). Plasticity in salt tolerance traits allows for invasion of novel habitat by Japanese knotweed s. l. (Fallopia japonica and F-bohemica, Polygonaceae). Am. J. Bot., 95, 931-942.
71. Richardson, D.M., Pyšek, P., Rejmanek, M., Barbour, M.G., Panetta, F.D. & West, C.J. (2000). Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib., 6, 93-107.
72. Ridley, C.E. & Ellstrand, N.C. (2009). Evolution of enhanced reproduction in the hybrid-derived invasive, California wild radish (Raphanus sativus). Biol. Invasions, 11, 2251-2264.
73. Rieseberg, L.H., Archer, M.A. & Wayne, R.K. (1999). Transgressive segregation, adaptation and speciation. Heredity, 83, 363-372.
74. Rieseberg, L.H., Kim, S.C., Randell, R.A., Whitney, K.D., Gross, B.L., Lexer, C. et al. (2007). Hybridization and the colonization of novel habitats by annual sunflowers. Genetica, 129, 149-165.
75. Rosenberg, M.S., Rothstein, H.R. & Gurevitch, J. (2013). Effect sizes: conventional choices and calculations. In Handbook of Meta-Analysis in Ecology and Evolution. (eds Koricheva, J., Gurevitch, J., Mengersen, K.). Princeton University Press Princeton, NJ, pp. 61-71.
76. Rouifed, S., Puijalon, S., Viricel, M.R. & Piola, F. (2011). Achene buoyancy and germinability of the terrestrial invasive Fallopia x bohemica in aquatic environment: a new vector of dispersion? Ecoscience, 18, 79-84.
77. Ryan, M.E., Johnson, J.R. & Fitzpatrick, B.M. (2009). Invasive hybrid tiger salamander genotypes impact native amphibians. Proc. Natl Acad. Sci. USA, 106, 11166-11171.
78. Schierenbeck, K.A. & Ellstrand, N.C. (2009). Hybridization and the evolution of invasiveness in plants and other organisms. Biol. Invasions, 11, 1093-1105.
79. Schwenk, K., Brede, N. & Streit, B. (2008). Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philos Trans R Soc B: Biol Sci, 363, 2805-2811.
80. Snow, A.A., Uthus, K.L. & Culley, T.M. (2001). Fitness of hybrids between weedy and cultivated radish: implications for weed evolution. Ecol. Appl., 11, 934-943.
81. Snow, A.A., Culley, T.M., Campbell, L.G., Sweeney, P.M., Hegde, S.G. & Ellstrand, N.C. (2010). Long-term persistence of crop alleles in weedy populations of wild radish (Raphanus raphanistrum). New Phytol., 186, 537-548.
82. Stebbins, G.L. (1959). The role of hybridization in evolution. Proc. Am. Philos. Soc., 103, 231-251.
83. Stebbins, G.L. (1985). Polyploidy, hybridization, and the invasion of new habitats. Ann. Mo. Bot. Gard., 72, 824-832.
84. Sullivan, L., Wildova, R., Goldberg, D. & Vogel, C. (2010). Growth of three cattail (Typha) taxa in response to elevated CO(2). Plant Ecol., 207, 121-129.
85. Sun, J., Qian, Q., Ma, D.R., Xu, Z.J., Liu, D., Du, H.B. et al. (2013). Introgression and selection shaping the genome and adaptive loci of weedy rice in northern China. New Phytol., 197, 290-299.
86. Tavalire, H.F., Bugbee, G.E., LaRue, E.A. & Thum, R.A. (2012). Hybridization, cryptic diversity, and invasiveness in introduced variable-leaf watermilfoil. Evol. Appl., 5, 892-900.
87. Urbanska, K.M., Hurka, H., Landolt, E., Neuffer, B. & Mummenhoff, K. (1997). Hybridization and evolution in Cardamine (Brassicaceae) at Urnerboden, central Switzerland: biosystematic and molecular evidence. Plant Syst. Evol., 204, 233-256.
88. Van Grunsven, R.H.A., Bos, F., Ripley, B.S., Suehs, C.M. & Veenendaal, E.M. (2009). Release from soil pathogens plays an important role in the success of invasive Carpobrotus in the Mediterranean. South African J. Botany, 75, 172-175.
89. Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. J. Stat. Softw., 36, 1-49.
90. Vila, M. & D'Antonio, C.M. (1998a). Fitness of invasive Carpobrotus (Aizoaceae) hybrids in coastal California. Ecoscience, 5, 191-199.
91. Vila, M. & D'Antonio, C.M. (1998b). Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecol. Appl., 8, 1196-1205.
92. Webb, C.O. & Donoghue, M.J. (2005). Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes, 5, 181-183. http://phylodiversity.net/phylomatic/.
93. Webb, C.O., Ackerly, D.D. & Kembel, S.W. (2008). Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics, 24, 2098-2100.
94. Weber, E. & D'Antonio, C.M. (1999). Phenotypic plasticity in hybridizing Carpobrotus spp. (Aizoaceae) from coastal California and its role in plant invasion. Can. J. Bot.-Revue Canadienne De Botanique, 77, 1411-1418.
95. Whitney, K.D., Randell, R.A. & Rieseberg, L.H. (2006). Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am. Naturalist, 167, 794-807.
96. Whitney, K.D., Ahern, J.R. & Campbell, L.G. (2009). Hybridization-prone plant families do not generate more invasive species. Biol. Invasions, 11, 1205-1215.
97. Whitney, K.D., Ahern, J.R., Campbell, L.G., Albert, L.P. & King, M.S. (2010a). Patterns of hybridization in plants. Perspectives in Plant Ecol. Evol. Systematics, 12, 175-182.
98. Whitney, K.D., Randell, R.A. & Rieseberg, L.H. (2010b). Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol., 187, 230-239.
99. Wikström, N., Savolainen, V. & Chame, M.W. (2001). Evolution of angiosperms: calibrating the family tree. Proc. Biol. Sci., 268, 2211-2220.
100. Wu, W., Zhou, R.C., Ni, G.Y., Shen, H. & Ge, X.J. (2013). Is a new invasive herb emerging? Molecular confirmation and preliminary evaluation of natural hybridization between the invasive Sphagneticola trilobata (Asteraceae) and its native congener S-calendulacea in South China. Biol. Invasions, 15, 75-88.