Advertisement

Evolutionary Ecology

, Volume 33, Issue 3, pp 345–367 | Cite as

Flower colour divergence is associated with post-fire regeneration dimorphism in the fynbos heath Erica coccinea subsp. coccinea (Ericaceae)

  • Fernando OjedaEmail author
  • Jeremy Midgley
  • Anton Pauw
  • Anu Lavola
  • Ramón Casimiro-Soriguer
  • Dawood Hattas
  • José Gabriel Segarra-Moragues
  • Riitta Julkunen-Tiitto
Original Paper

Abstract

The South African Cape fynbos heath Erica coccinea subsp. coccinea is polymorphic for post-fire regeneration mode (seeder/resprouter), flower colour (red/yellow), flowering time (summer-autumn/winter-spring), as well as anther size. These polymorphisms tend to occur between, rather than within, populations. Here, we aimed to understand flower colour divergence in this fynbos heath species and its association with post-fire regeneration. We tested for an association between these polymorphisms. We also examined whether yellow-flowered plants lacked anthocyanins and whether the lack of anthocyanins affected the concentration of other flavonoids, both in flowers and shoots. We found a strong association between flower colour, regeneration mode and flowering phenology. We also detected larger anthers and larger pollen in yellow- than in red-flowered plants, consistently for both resprouter and seeder regeneration strategies. Finally, we ascertained that being yellow-flowered is associated with loss in the capacity of synthesizing anthocyanins in both the flower and in the vegetative tissue. Considering that pollinator availability or preferences do probably not constitute a selection pressure, we propose that both enhanced reproductive success of anthocyaninless, yellow-flowered plants and the avoidance of likely negative pleiotropic effects (early senescence) in seeders would be key to understanding the flower colour divergence in E. coccinea subsp. coccinea.

Keywords

Anthocyanins Flavonols Flower colour polymorphism Increased male function Negative pleiotropic effects Resprouter Seeder 

Notes

Acknowledgements

Cape Nature and SANPARKS issued the necessary permits for fieldwork. F.O. strongly thanks the Spanish Ministerio de Educación (travel Grant PR2010-0365) and the UCA Plan Propio de Investigación (University of Cádiz; EST2016022) for providing travelling bursaries to do fieldwork.

Author contributions

F.O. planned and designed the research, conducted fieldwork and analysed data. R.C.S. carried out and wrote the Methods for pollen measurements. A.L., D.H. and R.J.-T. performed flavonoid analyses and contributed to write the “Methods” section. J.G.S.-M. performed the genetic analyses. F.O. wrote the manuscript and J.M., A.P. and J.G.S.-M. contributed to the discussion.

Funding

This study was conducted with funds from the Spanish Ministerio de Educación (travel Grant PR2010-0365) and the UCA Plan Propio de Investigación (University of Cádiz; EST2016022).

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.

Supplementary material

10682_2019_9985_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 32 kb)
10682_2019_9985_MOESM2_ESM.docx (146 kb)
Supplementary material 2 (DOCX 146 kb)
10682_2019_9985_MOESM3_ESM.csv (60 kb)
Supplementary material 3 (CSV 59 kb)

References

  1. Bates D, Maechler M, Bolker B (2013) Lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2. http://CRAN.R-project.org/package=lme4. Accessed Aug–Sep 2016
  2. Bell TL, Ojeda F (1999) Underground starch storage in Erica species of the Cape Floristic Region—differences between seeders and resprouters. New Phytol 144:143–152CrossRefGoogle Scholar
  3. Bi X, Zhang J, Chen C, Zhang D, Li P, Ma F (2014) Anthocyanin contributes more to hydrogen peroxide scavenging than other phenolics in apple peel. Food Chem 152:205–209CrossRefPubMedGoogle Scholar
  4. Carlson JE, Holsinger KE (2010) Natural selection on inflorescence color polymorphisms in wild Protea populations: the role of pollinators, seed predators, and intertrait correlations. Am J Bot 97:934–944CrossRefPubMedGoogle Scholar
  5. Carlson JE, Holsinger KE (2013) Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub. Oecologia 171:905–919CrossRefPubMedGoogle Scholar
  6. Casimiro-Soriguer I, Narbona E, Buide ML, del Valle JC, Whittall JB (2016) Transcriptome and biochemical analysis of a flower color polymorphism in Silene littorea (Caryophyllaceae). Front Plant Sci 7:204CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cavaiuolo M, Cocetta G, Ferrante A (2013) The antioxidants changes in ornamental flowers during development and senescence. Antioxidants 2:132–155CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chesson P (2000) Mechanisms of maintenance of species diversity. Ann Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  9. Combs JK, Pauw A (2009) Preliminary evidence that the long-proboscid fly Philoliche gulosa pollinates Disa karooica and its proposed Batesian model Pelargonium stipulaceum. S Afr J Bot 75:757–761CrossRefGoogle Scholar
  10. Crawley MJ (2013) The R book, 2nd edn. Wiley, ChichesterGoogle Scholar
  11. Crowden RK, Jarman SJ (1976) Anthocyanins in the genus Erica. Phytochemistry 15:1796–1797CrossRefGoogle Scholar
  12. Delph LF, Galloway LF, Stanton ML (1996) Sexual dimorphism in flower size. Am Nat 148:299–320CrossRefGoogle Scholar
  13. Di Ferdinando M, Brunetti C, Agati G, Tattini M (2014) Multiple functions of polyphenols in plants inhabiting unfavorable Mediterranean areas. Environ Exp Bot 103:107–116CrossRefGoogle Scholar
  14. Dreyer DL, Jones KC (1981) Feeding deterrency of flavonoidsand related phenolicstowards Schizaphis graminum and Myzus persicae: aphid feeding deterrents in wheat. Phytochemistry 20:2489–2493CrossRefGoogle Scholar
  15. Eckhart VM, Rushing NS, Hart GM, Hansen JD (2006) Frequency—dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:412–421CrossRefGoogle Scholar
  16. Esfeld K, Berardi AE, Moser M, Bossolini E, Freitas L, Kuhlemeier C (2018) Pseudogenization and resurrection of a speciation gene. Curr Biol 28:3776–3786CrossRefPubMedGoogle Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  18. Falcone-Ferreyra ML, Rius S, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222PubMedPubMedCentralGoogle Scholar
  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  20. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Ann Rev Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  21. Frey FM (2004) Opposing natural selection from herbivores and pathogens may maintain floral-color variation in Claytonia virginica (Portulacaceae). Evolution 58:2426–2437CrossRefPubMedGoogle Scholar
  22. Gigord LDB, Macnair MR, Smithson A (2001) Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soò. Proc Natl Acad Sci USA 98:6253–6255CrossRefPubMedGoogle Scholar
  23. Gou J-Y, Felippes FF, Liu C-J, Weigel D, Wang J-W (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522CrossRefPubMedPubMedCentralGoogle Scholar
  24. Heystek A, Geerts S, Barnard P, Pauw P (2014) Pink flower preference in sunbirds does not translate into plant fitness differences in a polymorphic Erica species. Evol Ecol 28:457–471CrossRefGoogle Scholar
  25. Hockey PAR, Dean WRJ, Ryan PG (2005) Roberts birds of Southern Africa, 7th edn. The Trustees of the John Voelcker Bird Book Fund, Cape TownGoogle Scholar
  26. Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G (2003) The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84:1733–1743CrossRefGoogle Scholar
  27. Johnson SD (2010) The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos Trans R Soc B 365:499–516CrossRefGoogle Scholar
  28. Julkunen-Tiitto R, Sorsa S (2001) Testing the drying methods for willow flavonoids, tannins and salicylates. J Chem Ecol 27:779–789CrossRefPubMedGoogle Scholar
  29. Kay KM, Sargent RD (2009) The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Ann Rev Ecol Evol Syst 40:637–656CrossRefGoogle Scholar
  30. Kikuzawa K, Lechowicz MJ (2018) Leaf Photosynthesis Integrated over Time. In: Adams W III, Terashima I (eds) The leaf: a platform for performing photosynthesis. Advances in photosynthesis and respiration (including bioenergy and related processes), vol 44. Springer, Cham, pp 473–492CrossRefGoogle Scholar
  31. Klaper R, Frankel S, Berenbaum MR (1996) Anthocyanin content and UV-B sensitivity in Brassica rapa. Photochem Photobiol 63:811–813CrossRefGoogle Scholar
  32. Kosonen M, Lännenpää M, Ratilainen M, Kontunen-Soppela S, Julkunen-Tiitto R (2015) Decreased anthocyanidin reductase (ANR) expression strongly decreases silver birch (Betula pendula) growth and alters phenolics accumulation. Physiol Plant 155:384–399CrossRefPubMedGoogle Scholar
  33. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Mol Biol Evol 3:1870–1874CrossRefGoogle Scholar
  34. Lamborn E, Cresswell JE, Macnair MR (2005) The potential for adaptive evolution of pollen grain size in Mimulus guttatus. New Phytol 167:289–296CrossRefPubMedGoogle Scholar
  35. Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17CrossRefGoogle Scholar
  36. Langella O (2000) Populations (Logiciel de genétique des populations). CNRS, ParisGoogle Scholar
  37. Larter M, Dunbar-Wallis A, Berardi AE, Smith SD (2018) Convergent evolution at the pathway level: predictable regulatory changes during flower color transitions. Mol Biol Evol 35:2159–2169CrossRefGoogle Scholar
  38. Lavola A, Karjalainen R, Julkunen-Tiitto R (2012) Bioactive polyphenols in leaves, stems, and berries of Saskatoon (Amelanchier alnifolia Nutt.) cultivars. J Agric Food Chem 60:1020–1027CrossRefPubMedGoogle Scholar
  39. Leonard J, West AG, Ojeda F (2018) Differences in germination response to smoke and temperature cues in ‘pyrophyte’ and ‘pyrofuge’ forms of Erica coccinea (Ericaceae). Int J Wildland Fire 27:562–568CrossRefGoogle Scholar
  40. Malan M (2013) Intraspecific variation in Erica coccinea. M.Sc. thesis, University of Cape Town, Cape TownGoogle Scholar
  41. McCallum B, Chang S-M (2016) Pollen competition in style: effects of pollen size on siring success in the hermaphroditic common morning glory, Ipomoea purpurea. Am J Bot 103:460–470CrossRefPubMedGoogle Scholar
  42. Munné-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13:216–220CrossRefPubMedGoogle Scholar
  43. Nakabayashi R, Yamazaki M, Saito K (2010) A polyhedral approach for understanding flavonoid biosynthesis in Arabidopsis. New Biotechnol 27:829–836CrossRefGoogle Scholar
  44. Narbona E, Wang H, Ortiz PL, Arista M, Imbert E (2018) Flower colour polymorphism in the Mediterranean Basin: occurrence, maintenance and implications for speciation. Plant Biol 20:8–20CrossRefPubMedGoogle Scholar
  45. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170CrossRefPubMedGoogle Scholar
  46. Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant activities of red versus green leaves in Elatostema rugosum. Plant Cell Environ 25:539–547CrossRefGoogle Scholar
  47. Newman E, Anderson B, Johnson SD (2012) Flower colour adaptation in a mimetic orchid. Proc R Soc Lond B Biol Sci 279:2309–2313CrossRefGoogle Scholar
  48. Ntalli NG, Caboni P (2012) Botanical nematicides: a review. J Agric Food Chem 60:9929–9940CrossRefPubMedGoogle Scholar
  49. Ojeda F, Brun FG, Vergara JJ (2005) Fire, rain, and the selection of seeder and resprouter life-histories in fire-recruiting, woody plants. New Phytol 168:155–165CrossRefPubMedGoogle Scholar
  50. Ojeda F, Budde KB, Heuertz M, Segarra-Moragues JG, González-Martínez S (2016a) Biogeography and evolution of seeder and resprouter forms of Erica coccinea (Ericaceae) in the fire-prone Cape fynbos. Plant Ecol 217:751–761CrossRefGoogle Scholar
  51. Ojeda F, van der Niet T, Malan MC, Midgley JJ, Segarra-Moragues JG (2016b) Strong signature of selection in seeder populations but not in resprouters of the fynbos heath Erica coccinea (Ericaceae). Bot J Linn Soc 181:115–126CrossRefGoogle Scholar
  52. Oliver EGH, Oliver IM (2002) The genus Erica (Ericaceae) in southern Africa: taxonomic notes 1. Bothalia 32:37–61Google Scholar
  53. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, van Loon JJA, Dicke M (2014) Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. J Exp Bot 65:2203–2217CrossRefPubMedPubMedCentralGoogle Scholar
  54. Page M, Sultana N, Paszkiewicz K, Florance H, Smirnoff N (2012) The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. Plant Cell Environ 35:388–404CrossRefPubMedGoogle Scholar
  55. Pausas JG, Bradstock RA, Keith DA, Keeley JA (2004) Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85:1085–1100CrossRefGoogle Scholar
  56. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2011) Nlme: linear and nonlinear mixed effects models. R package version 3.1-98Google Scholar
  57. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  58. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  59. Rausher MD (2006) The evolution of flavonoids and their genes. In: Grotewold E (ed) The science of flavonoids. Springer, Berlin, pp 175–211CrossRefGoogle Scholar
  60. Rausher MD (2008) Evolutionary transitions in floral color. Int J Plant Sci 169:7–21CrossRefGoogle Scholar
  61. Rebelo AG, Siegfried WR (1985) Colour and size of flowers in relation to pollination of Erica species. Oecologia 65:584–590CrossRefPubMedGoogle Scholar
  62. Rebelo AG, Siegfried WR, Oliver EGH (1985) Pollination syndromes of Erica species in the south-western Cape. S Afr J Bot 51:270–280CrossRefGoogle Scholar
  63. Sarkissian T, Harder L (2001) Direct and indirect responses to selection on pollen size in Brassica rapa L. J Evol Biol 14:456–468CrossRefGoogle Scholar
  64. Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315CrossRefGoogle Scholar
  65. Segarra-Moragues JG, Ojeda F (2010) Post-fire response and genetic diversity in Erica coccinea: connecting population dynamics and diversification in a biodiversity hotspot. Evolution 64:3511–3524CrossRefPubMedGoogle Scholar
  66. Segarra-Moragues JG, Donat-Caerols S, Ojeda F (2009) Isolation and characterization of microsatellite loci in the Cape fynbos heath Erica coccinea (Ericaceae). Conserv Genet 10:1815–1819CrossRefGoogle Scholar
  67. Shirley BW (1996) Flavonoid biosynthesis: ‘new’ functions for an ‘old’ pathway. Trends Plant Sci 1:377–382Google Scholar
  68. Sobel JM, Streisfeld MA (2013) Flower color as a model system for studies of plant evo-devo. Front Plant Sci 4:321CrossRefPubMedPubMedCentralGoogle Scholar
  69. Stanton ML (1987) Reproductive biology of petal colour variants in wild populations of Raphanus sativus. I. Pollinator response to colour morphs. Am J Bot 74:178–187CrossRefGoogle Scholar
  70. Stanton ML (1994) Male–male competition during pollination in plant populations. Am Nat 144:840–868CrossRefGoogle Scholar
  71. Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361CrossRefGoogle Scholar
  72. Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University, Oxford, pp 120–138Google Scholar
  73. Streisfeld MA, Kohn JR (2007) Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J Evol Biol 20:122–132CrossRefPubMedGoogle Scholar
  74. Streisfeld MA, Rausher MD (2009) Altered trans-regulatory control of gene expression in multiple anthocyanin genes contributes to adaptive flower color evolution in Mimulus aurantiacus. Mol Biol Evol 26:433–444CrossRefPubMedGoogle Scholar
  75. Tanaka Y, Brugliera F (2013) Flower colour and cytochromes P450. Philos Trans R Soc B 368:20120432CrossRefGoogle Scholar
  76. Tanaka Y, Sasaki N, Ohmiya A (2008) Plant pigments for coloration: anthocyanins, betalains and carotenoids. Plant J 54:733–749CrossRefPubMedGoogle Scholar
  77. Tanaka Y, Brugliera F, Kalc G, Senior M, Dyson B, Nakamura N, Katsumoto Y, Chandler S (2010) Flower color modification by engineering of the flavonoid biosynthetic pathway: practical perspectives. Biosci Biotechnol Biochem 74:1760–1769CrossRefPubMedGoogle Scholar
  78. Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323CrossRefPubMedGoogle Scholar
  79. Thairu MW, Brunet J (2015) The role of pollinators in maintaining variation in flower colour in the Rocky Mountain columbine, Aquilegia coerulea. Ann Bot 115:971–979CrossRefPubMedPubMedCentralGoogle Scholar
  80. Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591CrossRefPubMedGoogle Scholar
  81. Van der Niet T, Pirie MD, Shuttleworth A, Johnson SD, Midgley JJ (2014) Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii? Ann Bot 113:301–315CrossRefPubMedGoogle Scholar
  82. van Wilgen BW (1987) Fire regimes in the fynbos biome. In: Cowling RM, Le Maitre DC, McKenzie B, Prys-Jones RP, van Wilgen BW (eds) Disturbance and the dynamics of fynbos biome communities. South African national scientific programmes report 135. Foundation for Research Development, Pretoria, pp 6–14Google Scholar
  83. Verdaguer D, Ojeda F (2002) Root starch storage and allocation patterns in seeder and resprouter seedlings of two Cape Erica (Ericaceae) species. Am J Bot 89:1189–1196CrossRefPubMedGoogle Scholar
  84. Verdaguer D, Ojeda F (2005) Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds. Ann Bot 95:593–599CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wang Y, Siemann E, Wheeler GS, Zhu L, Gu X, Ding J (2012) Genetic variation in anti-herbivore chemical defences in an invasive plant. J Ecol 100:894–904CrossRefGoogle Scholar
  86. Wessinger CA, Rausher MD (2012) Lessons from flower colour evolution on targets of selection. J Exp Bot 63:5741–5749CrossRefPubMedGoogle Scholar
  87. Whittall JB, Voelckel C, Kliebenstein DJ, Hodges SA (2006) Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Mol Ecol 15:4645–4657CrossRefPubMedGoogle Scholar
  88. Winkel BSJ (2006) The biosynthesis of flavonoids. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 71–95CrossRefGoogle Scholar
  89. Yuan YW, Byers KJRP, Bradshaw HD (2013) The genetic control of flower–pollinator specificity. Curr Opin Plant Biol 16:422–428CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zentgraf U, Doll J, Riester L (2018) Live and let die: the core circadian oscillator coordinates plant life history and pilots leaf senescence. Mol Plant 11:351–353CrossRefPubMedGoogle Scholar
  91. Zhang Q, Su LJ, Chen JW, Zeng XQ, Sun BY, Peng CL (2012) The antioxidative role of anthocyanins in Arabidopsis under high-irradiance. Biol Plant 56:97–104CrossRefGoogle Scholar
  92. Zhu M, Zheng X, Shu Q, Li H, Zhong P, Zhang H, Xu Y, Wang L, Wang L (2012) Relationship between the composition of flavonoids and flower colors variation in tropical Water Lily (Nymphaea) Cultivars. PLoS ONE 7:e3433Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Departamento de Biología - IVAGROUniversidad de CádizPuerto RealSpain
  2. 2.Department of Biological SciencesUniversity of Cape TownRondebosch, Cape TownSouth Africa
  3. 3.Department of Botany and ZoologyStellenbosch UniversityMatieland, StellenboschSouth Africa
  4. 4.Natural Product Research Laboratories, Department of Environmental and Biological SciencesUniversity of Eastern Finland (UEF)JoensuuFinland
  5. 5.Departmento de Botánica y Geología, Facultad de Ciencias BiológicasUniversidad de ValenciaBurjassotSpain

Personalised recommendations