Comparative labellum micromorphology of the sexually deceptive temperate orchid genus Ophrys: Diverse epidermal cell types and multiple origins of structural colour

Botanical Journal of the Linnean Society

Volumn 162, Issue 3, 2010, Pages 504-540

  Bradshaw, Elizabeth ^a,b   Rudall, Paula J ^a   Devey, Dion S ^a   Thomas, M Murphy ^a,c   Glover, Beverley J ^c   Bateman, Richard M ^a  

^a JODRELL LABORATORY   (United Kingdom)

^b NORWICH RESEARCH PARK   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Iridescence; Ontogeny; Phylogeny; Plant pollinator co evolution; Pollinator cues; Reflectivity; Scanning electron microscopy (SEM); Speciation; Species delimitation

Indexed keywords

COMPARATIVE STUDY; HERB; HYBRID; MICROMORPHOLOGY; MICROSCOPY; ONTOGENY; PHYLOGENETICS; PHYLOGENY; PLANT-POLLINATOR INTERACTION; SCANNING ELECTRON MICROSCOPY; SPECIATION (BIOLOGY);

OPHRYS; ORCHIDACEAE;

EID: 77952749496     PISSN: 00244074     EISSN: 10958339     Source Type: Journal    
DOI: 10.1111/j.1095-8339.2010.01033.x     Document Type: Article

References (106)

1. Aceto S, Caputo P, Cozzolino S, Gaudio L, Moretti A. Phylogeny and evolution of Orchis and allied genera based on ITS DNA variation: morphological gaps and molecular continuity. Molecular Phylogenetics and Evolution 1999, 13:67-76.
2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 2004, 16:2463-2480.
3. Royal horticultural society colour chart 1966, Anonymous, London, Royal Horticultural Society
4. Ascensão L, Francisco A, Cotrim H, Pais MS. Comparative structure of the labellum in Ophrys fusca and Ophrys lutea (Orchidaceae). American Journal of Botany 2005, 92:1059-1067.
5. Ayasse M, Schiestl FP, Paulus HF, Ibarra F, Francke W. Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proceedings of the Royal Society of London B 2003, 270:517-522.
6. Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W. Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 2000, 54:1999-2006.
7. Bateman RM. Evolution and classification of European orchids: insights from molecular and morphological characters. Journal Europäischer Orchideen 2001, 33:33-119.
8. Bateman RM. What's in a name? Journal of the Hardy Orchid Society 2009a, 6:88-99.
9. Bateman RM. Evolutionary classification of European orchids: the crucial importance of maximising explicit evidence and minimising authoritarian speculation. Journal Europäischer Orchideen 2009b, 41:501-572.
10. Bateman RM, Devey DS, Malmgren S, Bradshaw E, Rudall PJ. Conflicting species concepts underlie perennial taxonomic controversies in Ophrys. L'Orchidophile 2010, in press
11. Bateman RM, Hollingsworth PM, Preston J, Luo Y-B, Pridgeon AM, Chase MW. Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society 2003, 142:1-40.
12. Bateman RM, Pridgeon AM, Chase MW. Phylogenetics of subtribe Orchidinae (Orchidoideae, Orchidaceae) based on nuclear ITS sequences. 2. Infrageneric relationships and taxonomic revision to achieve monophyly of Orchis sensu stricto. Lindleyana 1997, 12:113-141.
13. Bateman RM, Rudall PJ. The Good, the Bad and the Ugly: using spontaneous terata to distinguish the possible from the impossible in orchid floral evolution. Aliso 2006, 22:481-496.
14. Bateman RM, Smith RJ, Fay MF. Morphometric and population-genetic analyses elucidate the origin, evolutionary significance and conservation implications of Orchis × angusticruris (O. purpurea × O. simia), a hybrid orchid new to Britain. Botanical Journal of the Linnean Society 2008, 157:687-711.
15. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin HL, Koes R, Roberts K, Martin C. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 2007, 134:1691-1701.
16. Bell AK, Roberts DL, Hawkins JA, Rudall PJ, Box MS, Bateman RM. Comparative micromorphology of nectariferous and nectarless labellar spurs in selected clades of subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society 2009, 160:369-387.
17. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yehremov A, Samuels L. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant Journal 2007, 52:485-498.
18. Borg-Karlson A. Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae). Phytochemistry 1990, 29:1359-1387.
19. Box MS, Bateman RM, Glover BJ, Rudall PJ. Floral ontogenetic evidence of repeated speciation via paedomorphosis in subtribe Orchidinae (Orchidaceae). Botanical Journal of the Linnean Society 2008, 157:429-454.
20. Bradshaw E. Comparative micromorophology of the sexually deceptive Ophrys flower, and the origin of its iridescent speculum. 2007, BSc thesis, University of Manchester
21. Brett DW, Sommerard AP. Ultrastructural development of plastids in the epidermis and starch layer of glossy Ranunculus petals. Annals of Botany 1986, 58:903-910.
22. Briscoe AD, Chittka L. The evolution of color vision in insects. Annual Review of Entomology 2001, 46:471-510.
23. Brodersen CR, Vogelmann TC. Do epidermal lens cells facilitate the absorptance of diffuse light? American Journal of Botany 2007, 94:1061-1066.
24. Cantone C, Sica M, Gaudio L, Aceto S. The OrcPI locus: genomic organization, expression pattern, and noncoding regions variability in Orchis italica (Orchidaceae) and related species. Gene 2009, 434:9-15.
25. Cortis P, Vereecken NJ, Schiestl FP, Barone Lumaga MR, Scrugli A, Cozzolino S. Pollinator and convergence and the nature of species boundaries in sympatric Sardinian Ophrys (Orchidaceae). Annals of Botany 2009, 104:497-506.
26. Cozzolino S, Scopece G. Specificity in pollination and consequences for postmating reproductive isolation in deceptive Mediterranean orchids. Transactions of the Royal Society of London B 2008, 363:3037-3046.
27. Cozzolino S, Widmer A. Orchid diversity: an evolutionary consequence of deception? Trends in Ecology and Evolution 2005a, 20:487-494.
28. Cozzolino S, Widmer A. The evolutionary basis of reproductive isolation in Mediterranean orchids. Taxon 2005b, 54:977-985.
29. D'Emerico S, Pignone D, Bartolo G, Pulvirenti S, Terrasi C, Stuto S, Scrugli A. Karyomorphology, heterochromatin patterns and evolution in the genus Ophrys (Orchidaceae). Botanical Journal of the Linnean Society 2005, 148:87-99.
30. Darwin C. On the various contrivances by which British and foreign orchids are fertilised by insects 1862, London, John Murray
31. Davies KL, Stpiczynska M, Turner MP. A rudimentary labellar speculum in Cymbidium lowianum (Rchb.f.) Rchb.f. and Cymbidium devonianum Paxton (Orchidaceae). Annals of Botany 2006, 97:975-984.
32. Delforge P. Orchids of Europe, North Africa and the Middle East 2006, 3rd, edn., London, A & C Black
33. Devey DS, Bateman RM, Fay MF, Hawkins JA. Friends or relatives? Phylogenetics and species delimitation in the controversial European orchid genus Ophrys. Annals of Botany 2008, 101:385-402.
34. Devey DS, Bateman RM, Fay MF, Hawkins JA. Genetic structure and systematic relationships within the Ophrys fuciflora aggregate (Orchidinae: Orchidaceae): high diversity in Kent and a wind-induced discontinuity bisecting the Adriatic. Annals of Botany 2009, 104:483-495.
35. Devillers P, Devillers-Terschuren J. Essai d'analyse systématique du genre Ophrys. Naturalistes Belges 1994, 75:273-400.
36. Di Stilio VS, Martin C, Schulfer AF, Connelly CF. An ortholog of MIXTA-like2 controls epidermal cell shape in flowers of Thalictrum. New Phytologist 2009, 183:718-728.
37. Ehrlinger JR, Bjorkman O. Pubescence and leaf spectral characteristics in a desert shrub, Encelia farinosa. Oecologia 1978, 36:151-162.
38. Galsterer S, Musso M, Asenbaum A, Furnkranz D. Reflectance measurements of glossy petals of Ranunculus lingua (Ranunculaceae) and of non-glossy petals of Heliopsis helianthoides (Asteraceae). Plant Biology 1999, 1:670-678.
39. Glover BJ, Perez-Rodriguez M, Martin C. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 1998, 125:3497-3508.
40. Godfery MJ. Classification of the genus Ophrys. Journal of Botany (London) 1928, 66:33-36.
41. Graham RM, Lee DW, Norstog K. Physical and ultrastructural basis of blue leaf iridescence in two neotropical ferns. American Journal of Botany 1993, 80:198-203.
42. Guldberg LD, Atsatt PR. Frequency of reflection and absorption of ultraviolet light in flowering plants. American Midland Naturalist 1974, 93:35-43.
43. Gulyás G, Sramkó G, Molnár AV, Rudnóy S, Illyés Z, Balázs T, Bratek Z. Nuclear ribosomal DNA ITS paralogs as evidence of recent interspecific hybridization in the genus Ophrys (Orchidaceae). Acta Biologica Cracoviensia Series Botanica 2005, 47:61-67.
44. Hemsley AR, Collinson ME, Kovach WL, Vincent B, Williams T. The role of self-assembly in biological systems: evidence from iridescent colloidal sporopollenin in Selaginella megaspore walls. Philosophical Transactions of the Royal Society B 1994, 345:163-173.
45. Herring PJ. Reflective systems in aquatic animals. Comparative Biochemistry and Physiology A 1994, 109:513-546.
46. Jersáková J, Johnson SD, Kindlmann P. Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews 2006, 81:213-235.
47. Johnson SD, Nilsson NA. Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology 1999, 80:2607-2618.
48. Kay QON, Daoud HS, Stirton CH. Pigment distribution, light reflection and cell structure in petals. Botanical Journal of the Linnean Society 1981, 83:57-84.
49. Kinoshita S, Yoshioka S. Structural colors in nature: the role of regularity and irregularity in the structure. ChemPhysChem 2005, 6:1442-1459.
50. Kinoshita S, Yoshioka S, Kawagoe K. Mechanisms of structural color in the Morpho butterfly: cooperation of regularity and irregularity in an iridescent scale. Proceedings of the Royal Society of London B 2002, 269:1417-1421.
51. Kullenberg B. Studies in Ophrys pollination. Zoologiska Bidrag från Uppsala 1961, 34:1-340.
52. Kunst L, Samuels AL. Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research 2003, 42:51-80.
53. Kurachi M, Takaku Y, Komiya Y, Hariyama T. The origin of extensive colour polymorphism in Plateucaris sericea (Chrysomelidae, Coleoptera). Naturwissenschaften 2001, 89:295-298.
54. Lee DW. Ultrastructural basis and function of iridescent blue colour of fruits in Elaeocarpus. Nature 1991, 349:260-262.
55. Malmgren S. Are there 25 or 250 Ophrys species? Journal of the Hardy Orchid Society 2008, 5:95-100.
56. Mant J, Peakall R, Schiestl FP. Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys? Evolution 2005, 59:1449-1463.
57. Mayden RL. A hierarchy of species concepts: the denouement in the saga of the species problem. Species: the units of biodiversity 1997, 381-421. Claridge MFDawah HAWilson MR. In, eds., London, Chapman & Hall
58. Meister R, Hallé M-A, Dumoulin H, Pieranski P. Structure of the cholesteric focal conic domains at the free surface. Physical Review E 1996, 54:3771-3782.
59. Micheneau C, Johnson SD, Fay MF. Orchid pollination: from Darwin to the present day. Botanical Journal of the Linnean Society 2009, 161:1-19.
60. Mondragón-Palomino M, Theissen G. MADS about the evolution of orchid flowers. Trends in Plant Science 2008, 13:51-59.
61. Mondragón-Palomino M, Theissen G. Why are orchid flowers so diverse? Reduction of evolutionary constraints by paralogues of class B floral homeotic genes. Annals of Botany 2009, 104:583-594.
62. Neville AC, Caveney S. Scarabeid beetle exocuticle as an optical analogue of cholesteric liquid crystals. Biological Reviews 1969, 44:531-562.
63. Noda K, Glover BJ, Linstead P, Martin C. Flower colour intensity depends on specialized cell shape controlled by a MYB-related transcription factor. Nature 1994, 369:661-664.
64. Parker AR. Diffracting optics in animals: diversity and biological significance. European Optical Society Topical Meeting Digest Series 1998, 18:27-30.
65. Parker AR, McKenzie DR, Large CJ. Multilayer reflectors in animals using green and gold beetles as con trasting examples. Journal of Experimental Biology 1998, 201:1307-1313.
66. Parkin J. The glossy petal of Ranunculus. Annals of Botany 1928, 42:739-755.
67. Parkin J. The structure of the starch layer in the glossy petal of Ranunculus. II. The British species examined. Annals of Botany 1935, 49:283-289.
68. Paulus HF. Deceived males - pollination biology of the Mediterranean orchid genus Ophrys. Journal Europäischer Orchideen 2006, 38:303-353.
69. Paulus HF, Gack C. Pollinators as prepollinating isolating factors: evolution and speciation in Ophrys (Orchidaceae). Israel Journal of Botany 1990, 39:43-97.
70. Pedersen H, Faurholdt N. Ophrys: the bee orchids of Europe 2007, Kew, Kew Publishing
71. Peitch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A 1992, 170:1432-1451.
72. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C. Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 2005, 132:359-370.
73. Pillon Y, Chase MW. Taxonomic exaggeration and its effects on orchid conservation. Conservation Biology 2007, 21:263-265.
74. Pridgeon AM, Bateman RM, Cox AV, Hapeman JR, Chase MW. Phylogenetics of the subtribe Orchidinae (Orchidoideae, Orchidaceae) based on nuclear ITS sequences. 1. Intergeneric relationships and polyphyly of Orchis sensu lato. Lindleyana 1997, 12:89-109.
75. Rudall PJ, Bateman RM. Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biological Reviews 2002, 77:403-441.
76. Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annual Review of Plant Biology 2008, 59:683-707.
77. Schiestl FP. On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 2005, 92:255-262.
78. Schiestl FP, Ayasse M. Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Systematics and Evolution 2002, 234:111-119.
79. Schiestl FP, Ayasse M, Paulus HF, Lofstedt C, Hansson BS, Ibarra F, Francke W. Orchid pollination by sexual swindle. Nature 1999, 399:421-422.
80. Schiestl FP, Ayasse M, Paulus HF, Lofstedt C, Hansson BS, Ibarra F, Francke W. Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deceit. Journal of Comparative Physiology A 2000, 186:567-574.
81. Schiestl FP, Cozzolino S. Evolution of sexual mimicry in the orchid subtribe Orchidinae: the role of preadaptations in the attraction of male bees as pollinators. BMC Evolutionary Biology 2008, 8:27. 10 pp.
82. Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Franke W. The chemistry of sexual deception in an orchid-wasp pollination system. Science 2003, 302:437-438.
83. Schlüter PM, Kohl G, Steussy TF, Paulus HF. A screen of low-copy nuclear genes reveals the LFY gene as phylogenetically informative in closely related species of orchids (Ophrys). Taxon 2007, 56:493-504.
84. Schlüter PM, Schiestl FP. Molecular mechanisms of floral mimicry in orchids. Trends in Plant Science 2008, 13:228-235.
85. Scopece G, Musacchio A, Widmer A, Cozzolino S. Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 2007, 61:2623-2642.
86. Scopece G, Musacchio A, Widmer A, Cozzolino S. Contrasting thoughts about deception in orchids: a response to Sobel & Randle. Evolution 2009, 63:2201-2204.
87. Servettaz O, Maleci LB, Grünanger P. Labellum micromorphology in the Ophrys bertolonii agg. and some related taxa (Orchidaceae). Plant Systematics and Evolution 1994, 189:123-131.
88. Sharma V, Crne M, Park JO, Srivassarao M. Structural origin of circularly polarized iridescence in jewelled beetles. Science 2009, 355:449-451.
89. Sobel JM, Randle A. Comparative approaches to the evolution of reproductive isolation: a comment on Scopece et al. 2009. Evolution 2009, 63:2201-2204.
90. Soliva M, Kocyan A, Widmer A. Molecular phylogenetics of the sexually deceptive orchid genus Ophrys (Orchidaceae) based on nuclear and chloroplast DNA sequences. Molecular Phylogenetics and Evolution 2001, 20:78-88.
91. Soliva M, Widmer A. Gene flow across species boundaries in sympatric, sexually deceptive Ophrys (Orchidaceae) species. Evolution 2003, 57:2252-2261.
92. Srinivasan MV, Lehrer M. Spatial acuity of honeybee vision and its spectral properties. Journal of Comparative Physiology A 1988, 162:159-172.
93. Stökl J, Paulus H, Dafni A, Schulz C, Francke W, Ayasse M. Pollinator attracting odour signals in sexually deceptive orchids of the Ophrys fusca group. Plant Systematics and Evolution 2005, 254:105-120.
94. Stökl J, Schlüter PM, Stuessy TF, Paulus HF, Assum G, Ayasse M. Scent variation and hybridization cause the displacement of a sexually deceptive orchid species. American Journal of Botany 2008, 95:472-481.
95. Stökl J, Schlüter PM, Stuessy TF, Paulus HF, Fraberger R, Erdmann D, Schulz C, Francke W, Assum G, Ayasse M. Speciation in sexually deceptive orchids: pollinator-driven selection maintains discrete odour phenotypes in hybridizing species. Biological Journal of the Linnean Society 2009, 98:439-451.
96. Strack D, Busch E, Klein E. Anthocyanin patterns in European orchids and their taxonomic and phylogenetic relevance. Phytochemistry 1989, 28:2127-2139.
97. Sundermann H. Europäische und mediterrane Orchideen - eine Bestimmungsflora 1980, 3rd, edn., Hildesheim, Schmersow
98. Thomas MM, Glover BJ, Ellis AG, Rudall PJ. Development of a complex floral trait: the pollinator-attracting petal spots of the beetle daisy, Gorteria diffusa (Asteraceae). American Journal of Botany 2009, 96:2184-2196.
99. Tsai W-C, Kuoh C-S, Chuang M-H, Chen W-H, Chen H-H. Four DEF-like MADS-box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiology 2004, 45:831-844.
100. Uphoff W. Anthocyanins in the flowers of European orchids. Experientia 1979, 35:1013-1014.
101. Uphoff W. Anthocyane und Evolution der europäischen Orchideen. Jahresberichte des naturwisschaftlichen Vereins in Wuppertal 1980, 33:123-135.
102. Véla E, Tirard A, Renusci M, Suehs CM, Provost E. Floral chemical signatures in the genus Ophrys L. (Orchidaceae): a preliminary test of a new tool for taxonomy and evolution. Plant Molecular Biology Reporter 2007, 25:83-97.
103. Vigneron JP, Rassart M, Vertesy Z, Kertesz K, Sarrazin M, Biro LP, Ertz D, Lousse V. Optical structure and function of the white filamentary hair covering the edelweiss bracts. Physical Review E 2005, 71:66-74.
104. Vukusic P, Sambles JR, Lawrence CR. Colour mixing in wing scales of a butterfly. Nature 2000, 404:457.
105. Vukusic P, Sambles JR, Lawrence CR, Wakely G. Sculpted-multilayer optical effects in two species of Papilio butterfly. Applied Optics 2001, 40:1116-1125.
106. Whitney HM, Kolle M, Andrew P, Chittka L, Steiner U, Glover BJ. Floral iridescence, produced by diffractive optics, acts as a cue for animal pollinators. Science 2009, 323:130-133.