Abstract
Despite numerous, well-documented evolutionary histories of plant groups which underwent rapid radiation in various oceanic archipelagos, very little is known about the genetic basis of species differences and adaptive radiation. This paper represents the first such study in the Macaronesian Islands using non-model endemic plants, the woody Sonchus alliance. Here I inferred the genetic basis of species differences between two Canary Island endemics, the herbaceous perennial, shade tolerant Lactucosonchus webbii and the woody, coastal desert perennial Sonchus radicatus by quantitative trait locus (QTL) mapping using AFLP markers. A total of 23 QTL (7.3–23.8% PVE; phenotypic variance explained) for 11 morphological traits were found, one for flowering time (31% PVE), and five QTL (7–10.7% PVE) for two physiological traits (intrinsic water use efficiency and stomatal conductance). Interpreted cautiously, these results suggest that major morphological and some physiological differences between the two species are controlled by numerous genes with small to moderate effect. This implies that major morphological changes in island plants can be more complex than suggested by other studies, such as in Tetramolopium in the Hawaiian Islands. The genetic basis of arborescence on islands, one of the most spectacular convergent features of plants across different lineages and archipelagos, is also discussed.
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References
Aldeidge A (1975) Taxonomic and anatomical studies in Sonchus L. subgenus Dendrosonchus Webb ex Schultz Bip. and related genera. PhD Dissertation, University of Reading, Reading, UK
Aldridge A (1979) Evolution within a single genus: Sonchus in Macaronesia. In: Bramwell D (ed) Plants and islands. Academic Press, New York, pp 279–290
Amasino RM (1996) Control of flowering time in plants. Curr Opin Genet Dev 6:480–487
Bachmann K (1983) Evolutionary genetics and the genetic control of morphogenesis in flowering plants. In: Hecht MK, Wallace B, Ghillean TP (eds) Evolutionary biology, vol 16. Plenum Press, New York, pp 157–208
Baldwin BG (1997) Adaptive radiation of the Hawaiian silversword alliance: congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, pp 103–128
Baldwin BG, Robichaux RH (1995) Historical biogeography and ecology of the Hawaiian silversword alliance (Asteraceae): new molecular phylogenetic perspectives. In: Wagner WL, Funk VA (eds) Hawaiian biogeography: evolution on a hot-spot archipelago. Smithsonian Institution Press, Washington, D.C., pp 259–287
Baldwin BG, Crawford DJ, Francisco-Ortega J, Kim S-C, Sang T, Stuessy TF (1998) Molecular phylogenetic insights on the origin and evolution of island plants. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants II. Kluwer, Massachusetts, pp 410–441
Barton N, Charlesworth B (1984) Genetic revolutions, founder effects, and speciation. Annu Rev Ecol Syst 15:133–164
Basten CJ, Weir BS, Zeng Z-B (2003) QTL Cartographer 1.17: a reference manual and tutorial for QTL mapping. Department of Statistics, North Carolina State University, Raleigh, NC
Battey N, Tooke F (2002) Molecular control and variation in the floral transition. Curr Opin Plant Biol 5:62–68
Böhle U-R, Hilger HH, Martin WF (1996) Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc Natl Acad Sci USA 93:11740–11745
Bohuon EJR, Ramsay LD, Craft JA, Arthur AE, Marshall DF, Lydiate DJ, Kearsey MJ (1998) The association of flowering time quantitative trait loci with duplicated regions and candidate loci in Brassica oleracea. Genetics 150:393–401
Boss PK, Bastow RW, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31
Bouck A, Wessler SR, Arnold ML (2007) QTL analysis of floral traits in Louisiana Iris hybrids. Evolution 61:2308–2319
Bradshaw HD Jr, Wilbert SM, Otto KG, Schemske DW (1995) Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376:762–765
Bradshaw HD Jr, Otto KG, Frewen BE, McKay JK, Schemske DW (1998) Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149:367–382
Bramwell D, Bramwell Z (2001) Wild flowers of the Canary Islands, 2nd edn. Editorial Rueda, Madrid
Burke JM, Tang S, Knapp SJ, Rieseberg LH (2002) Genetic analysis of sunflower domestication. Genetics 161:1257–1267
Carlquist S (1965) Island life. Natural History Press, New York
Carlquist S (1970) Hawaii: a natural history. Natural History Press, New York
Carlquist S (1974) Island biology. Natural History Press, New York
Charlesworth B, Lande R, Slatkin M (1982) A neo-Darwinian commentary on macroevolution. Evolution 36:474–498
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Coyne JJ (1992) Genetics and speciation. Nature 355:511–515
Crawford DJ, Stuessy TF, Silva OM (1987) Allozyme divergence and the evolution of Dendroseris (Compositae: Lactuceae) on the Juan Fernanadez Islands. Syst Bot 12:435–443
Dobzhabsky T (1937) Genetics and the origin of species. Columbia University Press, New York
Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075–1082
Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295
Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570
Doebley J, Stec A, Wendel JF, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc Natl Acad Sci USA 80:9888–9892
Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294
Donavan LA, Ehleringer JR (1994) Potential for selection on plants for water-use efficiency as estimated by carbon isotope discrimination. Am J Bot 81:927–935
Dorweiler J, Stec A, Kermicle K, Doebley J (1993) Teosinte glume architecture 1: a genetic locus controlling a key step in maize evolution. Science 262:233–235
Fenster CB, Ritland K (1994) Quantitative genetics of mating system divergence in the yellow monkeyflower species complex. Heredity 73:422–435
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Fisherman L, Kelly AJ, Willis JH (2002) Minor quantitative trait loci underlie flora traits associated with mating system divergence in Mimulus. Evolution 56:2138–2155
Francisco-Ortega J, Jansen RK, Santos-Guerra A (1996) Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora. Proc Natl Acad Sci USA 93:4085–4090
Francisco-Ortega J, Fuertes-Aguilar J, Kim S-C, Santos-Guerra A, Crawford DJ, Jansen RK (2002) Phylogeny of the Macaronesian endemic Crambe section Dendrocrambe (Brassicaceae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Am J Bot 89:1984–1990
Frary A, Nesbitt TC, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:88–95
Gailing O, Hombergen E-J, Bachmann K (1999) QTL mapping reveals specific genes for the evolutionary reduction of microsporangia in Microseris (Asteraceae). Plant Biol 1:219–225
Gibson AC (1998) Photosynthetic organs of desert plants. Bioscience 48:911–920
Givnish TJ (1998) Adaptive plant evolution on islands: classical patterns, molecular data, and new insights. In: Grant PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 281–304
Givnish TJ, Sytsma KJ, Hahn WJ, Smith JF (1995) Molecular evolution, adaptive radiation, and geographic speciation in Cyanea (Campanulaceae, Lobelioideae). In: Wagner WL, Funk VA (eds) Hawaiian biogeography: evolution on a hot-spot archipelago. Smithsonian Institution Press, Washington, D.C., pp 299–337
Gottlieb LD (1984) Genetics and morphological evolution in plants. Am Nat 123:681–709
Grandillo S, Tanksley SD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92:935–951
Grant V (1975) Genetics of flowering plants. Columbia University Press, New York
Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10:210–214
Groover AT, Robischon M (2006) Developmental mechanisms regulating secondary growth in woody plants. Curr Opin Plant Biol 9:55–58
Guy RD, Warne PG, Reid DM (1989) Stable carbon isotopes ratio as an index of water-use efficiency in C3 halophytes-possible relationships to strategies for osmotic adjustment. In: Rundel RW, Ehleringger JR, Nagy A (eds) Stable isotopes in ecological research. Springer, New York, pp 55–75
Handley LL, Robinson D, Scrimgeour CM, Gordeon D, Forester BP, Ellis RP, Nevo E (1997) Correlating molecular markers with physiological expression in Hordeum, developing approach using stable isotopes. New Phytol 137:159–163
Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455
Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347
Kim S-C (2007) Mapping unexplored genomes: a genetic linkage map of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian Islands. J Hered 98:293–299
Kim S-C, Rieseberg LH (1999) Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153:965–977
Kim S-C, Crawford DJ, Jansen RK (1996a) Phylogenetic relationships among the genera of the subtribe Sonchinae (Lactuceae: Asteraceae): evidence from ITS sequences. Syst Bot 21:417–432
Kim S-C, Crawford DJ, Francisco-Ortega F, Santos-Guerra A (1996b) The common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proc Natl Acad Sci USA 93:7743–7748
Kim S-C, Crawford DJ, Francisco-Ortega J, Santos-Guerra A (1999) Adaptive radiation and genetic differentiation in the woody Sonchus alliance (Asteraceae: Lactuceae) in the Macaronesian islands. Plant Syst Evol 215:101–118
Kim S-C, McGowen MR, Lubinsky P, Barber JC, Mort ME, Santos-Guerra A (2008) Timing and tempo of early and successive adaptive radiations in Macaronesia. PLoS ONE 3(5):e2139
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 49:345–370
Kuittinen H, Sillanpaa MJ, Savolainen O (1997) Genetic basis of adaptation: flowering time in Arabidopsis thaliana. Theor Appl Genet 95:573–583
Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Lee C, Kim S-C, Lundy K, Santos-Guerra A (2005) Chloroplast DNA phylogeny of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian Islands. Am J Bot 92:2072–2085
Lexer C, Rosenthal DM, Raymond O, Donovan LA, Rieseberg LH (2005) Genetics of species differences in the wild annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 169:2225–2239
Li ZK, Yu SB, Lafitte HR, Huang N, Courtois B, Hittalmani S, Vijayakumar CHM, Liu GF, Wang GC, Shashidhar HE, Zhuang JY, Zheng KL, Singh VP, Sidhu JS, Srivantaneeyakul S, Khush GS (2003) QTL × environment interactions in rice. I. Heading date and plant height. Theor Appl Genet 108:141–153
Lin J-Z, Ritland K (1997) Quantitative trait loci differentiating the outbreeding Mimulus guttatus from the inbreeding M. platycalyx. Genetics 146:1115–1121
Lin Y-R, Schertz KF, Paterson AH (1995) Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum population. Genetics 141:391–411
Lincoln SE, Daly MJ, Lander ES (1992) Mapping genes controlling quantitative traits with MAPMAKER/QTL 1.1. Whitehead Institute Technical Report, Cambridge, MA, pp 1–73
Liu JP, Van Eck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA 99:13302–13306
Macnair MR (1983) The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50:283–293
Macnair MR, Christie P (1983) Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus? Heredity 50:295–302
Macnair MR, Cumbes QJ (1989) The genetic architecture of interspecific variation in Mimulus. Genetics 122:211–222
Martin B, Nienhuis J, King G, Schaefer A (1989) Restriction fragment length polymorphisms associated with water-use efficiency in tomato. Science 243:1725–1728
Maynard Smith JA (1983) The genetics of stasis and punctuation. Annu Rev Genet 17:11–25
Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 40:1489–1492
Mitchell-Olds T (1995) The molecular basis of quantitative variation in natural populations. Trends Ecol Evol 10:324–328
Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111–S130
Orr A (1998) The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935–949
Orr A, Coyne JA (1992) The genetics of adaptation revisited. Am Nat 140:725–742
Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into Mendelian factors, using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726
Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216
Stebbins GL Jr (1975) Flowering plants: evolution above the species level. Harvard University Press, Cambridge
Stratton DA (1998) Reaction norm functions and QTL-environment interactions for flowering time in Arabidopsis thaliana. Heredity 81:144–155
Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–233
Taylor SJ, Arnold M, Martin NH (2009) The genetic architecture of reproductive isolation in Louisiana irises: hybrid fitness in nature. Evolution 63:2581–2594
Templeton AR (1981) Mechanisms of speciation—a population genetic approach. Annu Rev Ecol Syst 12:23–48
Thomas H, Thomas HM, Ougham H (2000) Annuality, perenniality and cell death. J Exp Bot 51:1781–1788
Turner JRG (1981) Adaptation and evolution in Heliconius: a defense of neo-Darwinian. Annu Rev Ecol Syst 12:99–121
van der Knaap E, Tanksley SD (2003) The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in Yellow Stuffer tomato. Theor Appl Genet 107:139–147
Van Houten W, Van Raamsdonk L, Bachmann K (1994) Interspecific evolution of Microseris pygmaea (Asteraceae, Lactuceae) analyzed by cosegregation of phenotypic characters (QTLs) and molecular markers (RAPDs). Plant Syst Evol 190:49–67
Vlot EC, Van Houten WH, Mauthe S, Bachmann K (1992) Genetic and nongenetic factors influencing deviations from five pappus parts in a hybrid between Microseris douglasii and M. bigelovii (Asteraceae, Lactuceae). Int J Plant Sci 153:89–97
Wang H, Zhang Y-M, Li X, Masinde GL, Mohan S, Baylink DJ, Xu S (2005) Bayesian shrinkage estimation of quantitative trait loci parameters. Genetics 170:465–480
Wegner KM, Berenos C, Schmid-Hempel P (2008) Nonadditive genetic components in resistance of the red flour beetle Tribolium castanaeum against parasite infection. Evolution 62:2381–2392
Westerbergh A, Doebley J (2002) Morphological traits defining species differences in wild relatives of maize are controlled by multiple quantitative trait loci. Evolution 56:273–283
Whitkus R (1998) Genetics of adaptive radiation in Hawaiian and Cook Islands species of Tetramolopium (Asteraceae). II. Genetic linkage map and its implications for interspecific breeding barriers. Genetics 150:1209–1216
Whitkus R, Doan H, Lowrey TK (2000) Genetics of adaptive radiation in Hawaiian species of Tetramolopium (Asteraceae). III. Evolutionary genetics of sex expression. Heredity 85:37–42
Xu S, Yi N, Burke D, Galecki A, Miller RA (2003) An EM algorithm for mapping binary disease loci: application to fibrosarcoma in a four-way cross mouse family. Genet Res 82:127–138
Zeng Z-B (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Acknowledgments
I thank Vincent Weng for taking care of plants in the greenhouse. Ginger White and Helen Violi helped measuring phenotypic and some physiological traits. Shizhong Xu graciously helped the binary trait mapping. The analytical portion of this research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2010-0002611).
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Kim, SC. Mapping unexplored genomes II: genetic architecture of species differences in the woody Sonchus alliance (Asteraceae) in the Macaronesian Islands. J Plant Res 125, 125–136 (2012). https://doi.org/10.1007/s10265-011-0424-z
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DOI: https://doi.org/10.1007/s10265-011-0424-z