Abstract
The evolution of floral movement responding to pollination environments has long intrigued biologists. This has been mostly demonstrated in different species, but has as yet few explanations at the family level. Style curvature occurs in 23 species of eight genera among our observed and surveyed 52 species of 13 genera in the Malvaceae. To analyze the origin of style curvature in these species, we mapped this and correlated characters onto molecular phylogenetic trees that were constructed using the combination of the chloroplast DNA sequences of ndhF and the rpl16 intron. The results showed that style curvature evolved at least five times in species with herkogamous flowers. The occurrence of style curvature was associated with a shift to annual or perennial herbs with herkogamous flowers, which have similar ecological distributions with unpredictable pollinator environments. Style curvature appears to have evolved to facilitate delayed selfing if outcrossing fails under unpredictable pollination conditions.
Similar content being viewed by others
References
Ackerly DD (2003) Community assembly, niche conservation, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184
Akpan GA (2000) Cytogenetic characteristics and the breeding system in six Hibiscus species. Theor Appl Genet 100:315–318
Alverson WS, Whitlock BA, Nyffeler R, Bayer C, Baum DA (1999) Phylogeny of the core Malvales: evidence from ndhF sequence data. Am J Bot 86:1474–1486
Archibald JK, Mort ME, Wolfe AD (2005) Phylogenetic relationships within Zaluzianskya (Scrophulariaceae s.s., tribe Manuleeae): classification based on DNA sequences from multiple genomes and implications for character evolution and biogeography. Syst Bot 30:196–215
Armbruster WS, Baldwin BG (1998) Switch from specialized to generalized pollination. Nature 394:632
Barrett SCH (1998) The evolution of mating strategies in flowering plants. Trends Plant Sci 3:335–341
Barrett SCH (2003) Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philos Trans R Soc Lond B 358:991–1004
Barrett SCH (2008) Major evolutionary transitions in flowering plant reproduction: an overview. Int J Plant Sci 169:1–5
Barrett SCH, Harder LD (2005) The evolution of polymorphic sexual systems in daffodils (Narcissus). New Phytol 165:45–53
Baum DA, Small RL, Wendel JF (1998) Biogeography and floral evolution of Baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets. Syst Biol 47:181–207
Baum DA, Smith SD, Yen A, Alverson WS, Nyffeler R, Whitlock BA, Oldham RL (2004) Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. Am J Bot 91:1863–1871
Bayer C, Fay MF, de Bruijn AY, Savolainen V, Morton CM, Kubritzki K, Alverson WS, Chase MW (1999) Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: a combined analysis of plastid atpB and rbcL DNA sequences. Biol J Linn Soc 129:267–303
Buttrose MS, Grant WJR, Lott JNA (1977) Reversible curvature of style branches of Hibiscus trionum L., a pollination mechanism. Aust J Bot 25:567–570
Bynum MR, Smith WK (2001) Floral movements in response to thunderstorms improve reproductive effort in the alpine species Gentiana algida (Gentianaceae). Am J Bot 88:1088–1095
Church SA (2003) Molecular phylogenetics of Houstonia (Rubiaceae): descending aneuploidy and breeding system evolution in the radiation of the lineage across North American. Mol Phylogenet Evol 27:223–238
Crisp MD, Arroyo MTK, Cook LG, Gandolfo MA, Jordan GJ, McGlone MS, Weston PH, Westoby M, Wilf P, Linder HP (2009) Phylogenetic biome conservatism on a global scale. Nature 458:754–756
Cronn RC, Small RL, Haselkorn T, Wendel JF (2002) Rapid diversification of the cotton genus (Gossypium: Malvaceae) revealed by analysis of sixteen nuclear and chloroplast genes. Am J Bot 89:707–725
Culley TM (2002) Reproductive biology and delayed selfing in Viola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. Int J Plant Sci 163:113–122
Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Phylogenet Evol 14:733–740
Darwin C (1876) The effects of cross and self-fertilisation in the vegetable kingdom. John Murray, London
Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilized by insects. John Murray, London
Edwards J, Whitaker D, Klionsky S, Laskowski MJ (2005) A record-breaking pollen catapult. Nature 435:164
Elle E, Hare JD (2002) Environmentally induced variation in floral traits affects the mating system in Datura wrightii. Funct Ecol 16:79–88
Feng KM (1984) Flora. Science Press, Beijing (in Chinese)
Fetscher AE (2001) Resolution of male-female conflict in a hermaphroditic flower. Proc R Soc B: Biol Sci 268:525–529
Forbis TA, Floyd SK, de Queiroz A (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56:2112–2125
Friedman J, Barrett SCH (2008) A phylogenetic analysis of the evolution of wind pollination in the angiosperms. Int J Plant Sci 169:49–58
Goodwillie C (1999) Multiple origins of self-compatibility in Linanthus section Leptosiphon (Polemoniaceae): phylogenetic evidence from internal-transcribed-spacer sequence data. Evolution 53:1387–1395
Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Syst 36:47–79
Groeneveld KM (1989) World Wildlife Fund (Australia) project 65, conservation biology of the endangered species Hibiscus insularis: final report, January 1989. Commonwealth of Australia
Herlihy CR, Eckert CG (2002) Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416:320–323
Holsinger KE (1996) Pollination biology and the evolution of mating systems in flowering plants. Evol Biol 29:107–149
Ihlen PG, Ekman S (2002) Outline of phylogeny and character evolution in Rhizocarpon (Rhizocarpaceae, lichenized Ascomycota) based on nuclear ITS and mitochondrial SSU ribosomal DNA sequences. Biol J Linn Soc 77:535–546
Jobson RW, Playford J, Cameron KM, Albert VA (2003) Molecular phylogenetics of Lentibulariaceae inferred from plastid rps16 intron and trnL-F DNA sequences: implications for character evolution and biogeography. Syst Bot 28:157–171
Johnson LA, Soltis DE (1998) Assessing congruence: empirical examples from molecular data. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants 2: DNA sequencing. Kluwer, Boston, pp 297–348
Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942
Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247
Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887
Klips RA, Snow AA (1997) Delayed autonomous self-pollination in Hibiscus laevis (Malvaceae). Am J Bot 84:48–53
Koopman MM, Baum DA (2008) Phylogeny and biogeography of tribe Hibisceae (Malvaceae) on Madagascar. Syst Bot 33:364–374
Kress WJ, Liu AZ, Newman M, Li QJ (2005) The molecular phylogeny of Alpinia (Zingiberaceae): a complex and polyphyletic genus of Gingers. Am J Bot 92:167–178
Li Q, Xu Z, Xia Y, Kress WJ, Zhang L, Deng X, Gao J, Bai Z (2001) Flexible style that encourages outcrossing. Nature 410:432
Liu KW, Liu ZJ, Huang LQ, Li LQ, Chen LJ, Tang GD (2006) Self-fertilization strategy in an orchid. Nature 441:945–946
Maddison WP, Maddison DR (2000) MacClade version 4: analysis of phylogeny and character evolution. Sinauer, Sunderland
Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB (2004) Natural variation in expression of self-incompatibility in Arabidopsis thaliana: Implications for the evolution of selfing. Proc Natl Acad Sci USA 101:16070–16074
Peter CI, Johnson SD (2006) Doing the twist: a test of Darwin’s cross-pollination hypothesis for pollinium reconfiguration. Biol Lett 2:65–68
Pfeil BE, Brubaker CL, Craven LA, Crisp MD (2002) Phylogeny of Hibiscus and the tribe Hibisceae (Malvaceae) using chloroplast DNA sequences of ndhF and the rpl16 intron. Syst Bot 27:333–350
Pfeil BE, Brubaker CL, Craven LA, Crisp MD (2004) Paralogy and orthology in the Malvaceae rpb2 gene family: investigation of gene duplication in Hibiscus. Mol Biol Evol 21:1428–1437
Qu R, Li X, Luo Y, Dong M, Xu H, Chen X, Dafni A (2007) Wind-dragged corolla enhances self-pollination: a new mechanism of delayed self-pollination. Ann Bot 100:1155–1164
Ruan CJ, Qin P, He ZX (2004) Delayed autonomous selfing in Kosteletzkya virginica (Malvaceae). S Afr J Bot 70:640–645
Ruan CJ, Qin P, Xi YG (2005) Floral traits and pollination modes in Kosteletzkya virginica (Malvaceae). Belg J Bot 138:39–46
Ruan CJ, Zhou LJ, Zeng FY, Han RM, Qin Q, Lutts S, Saad L, Mahy G (2008) Contribution of delayed autonomous selfing to reproductive success in Kosteletzkya virginica (Malvaceae). Belg J Bot 141:3–13
Ruan CJ, Li H, Mopper S (2009a) Kosteletzkya virginica displays mixed mating system responding to pollinator environment despite strong inbreeding depression. Plant Ecol 203:183–193
Ruan CJ, Mopper S, Teixeira da Silva JA, Qin P, Shan Y (2009b) Context-dependent style curvature within flowers offers reproductive assurance under unpredictable pollinator environments. Plant Syst Evol 277:207–215
Ruan CJ, Teixeira da Silva JA, Qin P (2010) Style curvature and its adaptive significance in the Malvaceae. Plant Syst Evol 288:13–23
Schemske DW, Bradshaw HD Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96:11910–11915
Seed L, Vaughton G, Ramsey M (2006) Delayed autonomous selfing and inbreeding depression in the Australian annual Hibiscus trionum var. vesicarius (Malvaceae). Aust J Bot 54:27–34
Seelanan T, Schnabel A, Wendel JF (1997) Congruence and consensus in the cotton tribe (Malvaceae). Syst Bot 22:259–290
Small RL (2004) Phylogeny of Hibiscus sect. Muenchhusia (Malvaceae) based on chloroplast rpl16 and ndhF, and nuclear ITS and GBSSI sequences. Syst Bot 29:385–392
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486
Stebbins GL (1974) Flowering plants: evolution above the species level. Belknap, Cambridge
Stephens WC (1948) Kansas wild flowers. University of Kansas Press, Lawrence, KS
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland
Tang Y, Gilbert MG, Dorr LJ (2007) Floral of China. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis
Tate JA, Aguilar JF, Wagstaff SJ (2005) Phylogenetic relationships within the tribe Malveae (Malvaceae, subfamily Malvoideae) as inferred from ITS sequence data. Am J Bot 92:584–602
Till-Bottraud I, Wu L, Harding J (1990) Rapid evolution of life history traits in populations of Poa annua L. J Evol Biol 3:205–224
Truyens S, Arbo MM, Shore JS (2005) Phylogenetic relationships, chromosome and breeding system evolution in Turnera (Turneraceae): inferences from its sequence data. Am J Bot 92:1749–1758
Upchurch P (2008) Gondwanan break-up: legacies of a lost world? Trends Ecol Evol 23:229–236
Wang Y, Zhang D, Renner SS, Chen Z (2004) A new self-pollination mechanism. Nature 431:39–40
Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. N Z J Bot 24:163–178
Weller SG, Sakai AK (1999) Using phylogenetic approaches for the analysis of plant breeding system evolution. Annu Rev Ecol Syst 30:167–199
Wendel JF, Albert VA (1992) Phylogenetics of the cotton genus (Gossypium): character-state weighted parsimony analysis of chloroplast-DNA restriction site data and its systematic and biogeographic implications. Syst Bot 17:115–143
Zeng FY, Zhou LJ, Ruan CJ (2008) Comparative study on floral traits and breeding system of Hibiscus syriacus and H. trionum (in Chinese with English abstract). Guihaia 28:750–754
Acknowledgments
The authors thank Q.X. Hu, Z.S. Wang and M.W. Wang for their help in investigations on style curvature and floral structures. Funding for this work was provided by the National Natural Science Foundation of China (grant no. 30500071 to C.-J. Ruan).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ruan, CJ., Chen, SC., Li, Q. et al. Adaptive evolution of context-dependent style curvature in some species of the Malvaceae: a molecular phylogenetic approach. Plant Syst Evol 297, 57 (2011). https://doi.org/10.1007/s00606-011-0499-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-011-0499-y