Accessibility, constraint, and repetition in adaptive floral evolution

Developmental Biology

Volumn 419, Issue 1, 2016, Pages 175-183

  Wessinger, Carolyn A ^a   Hileman, Lena C ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Bias; Developmental constraint; Floral morphology; Gene duplication; Pleiotropy; Repeated evolution

Indexed keywords

ADAPTIVE FLORAL EVOLUTION; FLOWER DEVELOPMENT; FLOWER MORPHOLOGY; GENE DOSAGE; GENE DUPLICATION; GENETIC CORRELATION; GENETIC TRAIT; GENETIC VARIATION; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PLANT EVOLUTION; PLEIOTROPY; POLLINATION; PRIORITY JOURNAL; REVIEW; SELFING; ADAPTATION; BIOLOGICAL MODEL; CROSS BREEDING; EVOLUTION; FLOWER; GENE EXPRESSION REGULATION; GENETIC SELECTION; MOLECULAR EVOLUTION; PHYSIOLOGY; PLANT GENE;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; CROSSES, GENETIC; EVOLUTION, MOLECULAR; FLOWERS; GENE DUPLICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC PLEIOTROPY; GENETIC VARIATION; MODELS, BIOLOGICAL; PHENOTYPE; POLLINATION; SELECTION, GENETIC;

EID: 84975521088     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.05.003     Document Type: Review

References (68)

1. Arnold, S.J., Constraints on phenotypic evolution. Am. Nat. 140 (1992), S85–S107.
2. Arthur, W., Developmental drive: an important determinant of the direction of phenotypic evolution. Evol. Dev. 3 (2001), 271–278.
3. Ashman, T.-L., Majetic, C.J., Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96 (2006), 343–352.
4. Bissell, E.K., Diggle, P.K., Floral morphology in Nicotiana: architectural and temporal effects on phenotypic integration. Int. J. Plant Sci. 169 (2008), 225–240.
5. Bissell, E.K., Diggle, P.K., Modular genetic architecture of floral morphology in Nicotiana: quantitative genetic and comparative phenotypic approaches to floral integration. J. Evol. Biol. 23 (2010), 1744–1758.
6. Bowman, J.L., Smyth, D.R., Meyerowitz, E.M., Genetic interactions among floral homeotic genes of Arabidopsis. Development 112 (1991), 1–20.
7. Bradshaw, H.D. Jr., Wilbert, S.M., Otto, K.G., Schemske, D.W., Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376 (1995), 762–765.
8. Bradshaw, H.D. Jr., Otto, K.G., Frewen, B.E., McKay, J.K., Schemske, D.W., Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149 (1998), 367–382.
9. Brock, M.T., Kover, P.X., Weinig, C., Natural variation in GA1 associates with floral morphology in Arabidopsis thaliana. New Phytol. 195 (2012), 58–70.
10. Brock, M.T., Dechaine, J.M., Iniguez-Luy, F.L., Maloof, J.N., Stinchcombe, J.R., Weinig, C., Floral genetic architecture: an examination of QTL architecture underlying floral (co)variation across environments. Genetics 186 (2010), 1451–1465.
11. Carroll, S.B., Evolution at two levels: on genes and form. PLoS Biol., 3, 2005, e245.
12. Conner, J., Via, S., Patterns of phenotypic and genetic correlations among morphological and life history traits in wild radish Raphanus raphanistrum. Evolution 47 (1993), 704–711.
13. Conner, J., Sterling, A., Testing hypotheses of functional relationships: a comparative survey of correlation patterns among floral traits in five insect-pollinated plants. Am. J. Bot. 82 (1995), 1399–1406.
14. Conner, J.K., Genetic mechanisms of floral trait correlations in a natural population. Nature 420 (2002), 407–410.
15. Conner, J.K., Quantitative genetic approaches to evolutionary constraint: how useful?. Evolution 66 (2012), 3313–3320.
16. Conner, J.K., Sahli, H.F., Karoly, K., Tests of adaptation: functional studies of pollen removal and estimates of natural selection on anther position in wild radish. Ann. Bot. 103 (2009), 1547–1556.
17. Conner, J.K., Karoly, K., Stewart, C., Koelling, V.A., Sahli, H.F., Shaw, F.H., Rapid independent trait evolution despite a strong pleiotropic genetic correlation. Am. Nat. 178 (2011), 429–441.
18. Edwards, C.E., Weinig, C., The quantitative-genetic and QTL architecture of trait integration and modularity in Brassica rapa across simulated seasonal settings. Heredity 106 (2011), 661–677.
19. Elliott, R.C., Betzner, A.S., Huttner, E., Oakes, M.P., Tucker, W.Q., Gerentes, D., Perez, P., Smyth, D.R., AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8 (1996), 155–168.
20. Faegri, K., van der Pijl, L., The Principles of Pollination Ecology. 1979, Pergamon, New York.
21. Feng, G., Qin, Z., Yan, J., Zhang, X., Hu, Y., Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL. New Phytol. 191 (2011), 635–646.
22. Fenster, C.B., Ritland, K., Quantitative genetics of mating system divergence in the yellow monkeyflower species complex. Heredity 73 (1994), 422–435.
23. Ferris, K.G., Rushton, T., Greenlee, A.B., Toll, K., Blackman, B.K., Willis, J.H., Leaf shape evolution has a similar genetic architecture in three edaphic specialists within the Mimulus guttatus species complex. Ann. Bot. 116 (2015), 213–223.
24. Fishman, L., Kelly, A.J., Willis, J.H., Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56 (2002), 2138–2155.
25. Fishman, L., Stathos, A., Beardsley, P.M., Williams, C.F., Hill, J.P., The genetics of reproductive barriers in Mimulus (monkeyflowers). Evolution 67 (2013), 2547–2560.
26. Fishman, L., Beardsley, P.M., Stathos, A., Williams, C.F., Hill, J.P., The genetic architecture of traits associated with the evolution of self-pollination in Mimulus. New Phytol. 205 (2014), 907–917.
27. Futuyma, D.J., Evolutionary constraint and ecological consequences. Evolution 64 (2010), 1865–1884.
28. Goodwillie, C., Ritland, C., Ritland, K., The genetic basis of floral traits associated with mating system evolution in Leptosiphon (Polemoniaceae): an analysis of quantitative trait loci. Evolution 60 (2006), 491–504.
29. Hall, M.C., Basten, C.J., Willis, J.H., Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus. Genetics 172 (2006), 1829–1844.
30. Hermann, K., Klahre, U., Venail, J., Brandenburg, A., Kuhlemeier, C., The genetics of reproductive organ morphology in two Petunia species with contrasting pollination syndromes. Planta 241 (2015), 1241–1254.
31. Hermann, K., Klahre, U., Moser, M., Sheehan, H., Mandel, T., Kuhlemeier, C., Tight genetic linkage of prezygotic barrier loci creates a multifunctional speciation island in Petunia. Curr. Biol. 23 (2013), 873–877.
32. Hu, Y., Xie, Q., Chua, N.-H., The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15 (2003), 1951–1961.
33. Hu, Y., Poy, H.M., Chua, N.-H., The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J. 47 (2006), 1–9.
34. Juenger, T., Purugganan, M., Mackay, T.F.C., Quantitative trait loci for floral morphology in Arabidopsis thaliana. Genetics 156 (2000), 1379–1392.
35. Juenger, T., Perez-Perez, J.M., Bernal, S., Micol, J.L., Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture. Evol. Dev. 7 (2005), 259–271.
36. Kelly, J.K., Connecting QTLs to the G-matrix of evolutionary quantitative genetics. Evolution 63 (2009), 813–825.
37. Krizek, B.A., Anderson, J.T., Control of flower size. J. Exp. Bot. 64 (2013), 1427–1437.
38. Lande, R., Arnold, S.J., The measurement of selection on correlated characters. Evolution 37 (1983), 1210–1226.
39. Losos, J.B., Convergence, adaptation, and constraint. Evolution 65 (2011), 1827–1840.
40. Lynch, M., Walsh, B., Genetics and Analysis of Quantitative Traits, 1998, Sinauer, Sunderland, MA.
41. Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., Wolpert, L., Developmental constraints and evolution. Q. Rev. Biol. 6 (1985), 265–287.
42. Mizukami, Y., Fischer, R.L., Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc. Natl. Acad. Sci. USA 97 (2000), 942–947.
43. Nakazato, T., Rieseberg, L.H., Wood, T.E., The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae). Heredity 111 (2013), 227–237.
44. Qin, Z., Zhang, X., Zhang, X., Feng, G., Hu, Y., The Arabidopsis ORGAN SIZE RELATED 2 is involved in the regulation of cell expansion during organ growth. BMC Plant Biol., 14, 2014, 349.
45. Ramsay, N.A., Glover, B.J., MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10 (2005), 63–70.
46. Rausher, M.D., Evolutionary transitions in floral color. Int. J. Plant Sci. 169 (2008), 7–21.
47. Ritland, C., Ritland, K., Variation of sex allocation among eight taxa of the Mimulus guttatus species complex (Scrophulariaceae). Am. J. Bot. 76 (1989), 1731–1739.
48. Saddic, L.A., Huvermann, B., Bezhani, S., Su, Y., Winter, C.M., Kwon, C.S., Collum, R.P., Wagner, D., The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133 (2006), 1673–1682.
49. Schluter, D., Adaptive radiation along genetic lines of least resistance. Evolution 50 (1996), 1766–1774.
50. Scoville, A., Lee, Y.W., Willis, J.H., Kelly, J.K., Contribution of chromosomal polymorphisms to the G-matrix of Mimulus guttatus. New Phytol. 183 (2009), 803–815.
51. Sheehan, H., Moser, M., Klahre, U., Esfeld, K., Dell'Olivo, A., Mandel, T., Metzger, S., Vandenbussche, M., Freitas, L., Kuhlemeier, C., MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation. Nat. Genet., 2015, 10.1038/ng.3462.
52. Sicard, A., Thamm, A., Marona, C., Lee, Y.W., Wahl, V., Stinchcombe, J.R., Wright, S.I., Kappel, C., Lenhard, M., Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Curr. Biol. 24 (2014), 1880–1886.
53. Sinervo, B., Svensson, E., Correlational selection and the evolution of genomic architecture. Heredity 89 (2002), 329–338.
54. Slotte, T., Hazzouri, K.M., Stern, D., Andolfatto, P., Wright, S.I., Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66 (2012), 1360–1374.
55. Smith, S.D., Pleiotropy and the evolution of floral integration. New Phytol. 209 (2016), 80–85.
56. Sobel, J.M., Streisfeld, M.A., Flower color as a model system for studies of plant evo-devo. Front. Plant Sci., 4, 2013, 321.
57. Stebbins, G.L., Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Ann. Rev. Ecol. Syst. 1 (1970), 307–326.
58. Stebbins, G.L., Flowering Plants: Evolution Above the Species Level, 1974, Arnold, London.
59. Streisfeld, M.A., Rausher, M.D., Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65 (2011), 629–642.
60. Thomson, J.D., Wilson, P., Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. Int. J. Plant Sci. 169 (2008), 23–38.
61. Vlad, D., Kierzkowski, D., Rast, M.I., Vuolo, F., Ioio, R.D., Galinha, C., Gan, X., Hajheidari, M., Hay, A., Smith, R.S., Huijser, P., Bailey, C.D., Tsiantis, M., Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343 (2014), 780–783.
62. Wagner, G.P., Altenberg, L., Complex adaptations and the evolution of evolvability. Evolution 50 (1996), 967–976.
63. Wessinger, C.A., Rausher, M.D., Lessons from flower colour evolution on targets of selection. J. Exp. Bot. 63 (2012), 5741–5749.
64. Wessinger, C.A., Rausher, M.D., Genetic changes associated with flower color evolution in Penstemon barbatus. Evolution 68 (2014), 1058–1070.
65. Wessinger, C.A., Rausher, M.D., Ecological transition predictably associated with gene degeneration. Mol. Biol. Evol. 32 (2015), 347–354.
66. Wessinger, C.A., Hileman, L.C., Rausher, M.D., Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon. Philos. Trans. R. Soc. Lond., 369, 2014, 20130349.
67. Wu, C.A., Lowry, D.B., Cooley, A.M., Wright, K.M., Lee, Y.W., Willis, J.H., Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100 (2008), 220–230.
68. Zhang, R., Guo, C., Zhang, W., Wang, P., Lin, L., Duan, X., Du, Q., Zhao, L., Shan, H., Hodges, S.A., Kramer, E.M., Ren, Y., Kong, H., Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae). Proc. Natl. Acad. Sci. USA 110 (2013), 5074–5079.