Access

You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:

login

Log in to your personal account or through your institution.

Pollination Syndromes and Floral Specialization

Charles B. Fenster, W. Scott Armbruster, Paul Wilson, Michele R. Dudash and James D. Thomson
Annual Review of Ecology, Evolution, and Systematics
Vol. 35 (2004), pp. 375-403
Published by: Annual Reviews
Stable URL: http://www.jstor.org/stable/30034121
Page Count: 31
  • Download PDF
  • Cite this Item
Pollination Syndromes and Floral Specialization
We're having trouble loading this content. Download PDF instead.

Abstract

Floral evolution has often been associated with differences in pollination syndromes. Recently, this conceptual structure has been criticized on the grounds that flowers attract a broader spectrum of visitors than one might expect based on their syndromes and that flowers often diverge without excluding one type of pollinator in favor of another. Despite these criticisms, we show that pollination syndromes provide great utility in understanding the mechanisms of floral diversification. Our conclusions are based on the importance of organizing pollinators into functional groups according to presumed similarities in the selection pressures they exert. Furthermore, functional groups vary widely in their effectiveness as pollinators for particular plant species. Thus, although a plant may be visited by several functional groups, the relative selective pressures they exert will likely be very different. We discuss various methods of documenting selection on floral traits. Our review of the literature indicates overwhelming evidence that functional groups exert different selection pressures on floral traits. We also discuss the gaps in our knowledge of the mechanisms that underlie the evolution of pollination syndromes. In particular, we need more information about the relative importance of specific traits in pollination shifts, about what selective factors favor shifts between functional groups, about whether selection acts on traits independently or in combination, and about the role of history in pollination-syndrome evolution.

Notes and References

This item contains 215 references.

Literature Cited
  • Aigner PA. 2001. Optimality modeling and fit- ness trade-offs: When should plants become pollinator specialists? Oikos 95:177-84
  • Aigner PA. 2004. The evolution of specialized floral phenotypes in a fine-grained pollina- tion environment. In Specialization and Gen- eralization in Plant-Pollinator Interactions, ed. NM Waser, J Ollerton. Chicago: Univ. Chicago Press. In press
  • Armbruster WS. 1984. The role of resin in an- giosperm pollination: ecological and chem- ical considerations. Am. J. Bot. 71:1149- 60
  • Armbruster WS. 1985. Patterns of character di- vergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphor- biaceae). Evolution 39:733-52
  • Armbruster WS. 1986. Reproductive inter- actions between sympatric Dalechampia species: Are natural assemblages "random" or organized? Ecology 67:522-33
  • Armbruster WS. 1988. Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecol- ogy 69:1746-61
  • Armbruster WS. 1990. Estimating and testing the shapes of adaptive surfaces: the morphol- ogy and pollination of Dalechampia blos- soms. Am. Nat. 135:14-31
  • Armbruster WS. 1992. Phylogeny and the evolution of plant-animal interactions. Bio- Science 42:12-20
  • Armbruster WS. 1993. Evolution of plant pol- lination systems: hypotheses and tests with the neotropical vine Dalechampia. Evolution 47:1480-505
  • Armbruster WS. 1996a. Evolution of floral morphology and function: an integrative ap- proach to adaptation, constraint, and com- promise in Dalechampia (Euphorbiaceae). In Floral Biology: Studies on Floral Evo- lution in Animal-Pollinated Plants, ed. DG Lloyd, SCH Barrett, pp. 241-72. New York: Chapman & Hall
  • Armbruster WS. 1996b. Exaptation, adapta- tion, and homoplasy: evolution of ecolog- ical traits in Dalechampia. In Homoplasy: The Recurrence of Similarity in Evolution, ed. MJ Sanderson, L Hufford, pp. 227-43. New York: Academic
  • Armbruster WS. 1997. Exaptations link the evolution of plant-herbivore and plant-pol- linator interactions: a phylogenetic inquiry. Ecology 78:1661-74
  • Armbruster WS. 2002. Can indirect selection and genetic context contribute to trait diver- sification? A transition-probability study of blossom-color evolution in two genera. J. Evol. Biol. 15:468-86
  • Armbruster WS, Baldwin BG. 1998. Switch from specialized to generalized pollination. Nature 394:632
  • Armbruster WS, Di Stilio VS, Tuxill JD, Flores TC, Velasquez Runk JL. 1999. Covariance and decoupling of floral and vegetative traits in nine neotropical plants: a re-evaluation of Berg's correlation-pleiades concept. Am. J. Bot. 86:39-55
  • Armbruster WS, Edwards ME, Debevec EM. 1994. Character displacement generates as- semblage structure of Western Australian triggerplants (Stylidium). Ecology 75:315- 29
  • Armbruster WS, Fenster CB, Dudash MR. 2000. Pollination "principles" revisited: spe- cialization, pollination syndromes, and the evolution of flowers. Det Nor. Vidensk. Acad. I. Mat. Natur. Kl. Skr. Ny Ser. 39:179-200
  • Armbruster WS, Herzig AL. 1984. Partitioning and sharing of pollinators by four sympatric species of Dalechampia (Euphorbiaceae) in Panama. Ann. Mo. Bot. Gard. 71:1-16
  • Armbruster WS, Howard JJ, Clausen TP, De- bevec EM, Loquvam JC, et al. 1997. Do bio- chemical exaptations link evolution of plant defense and pollination systems? Histori- cal hypotheses and experimental tests with Dalechampia vines. Am. Nat. 149:461-84
  • Armbruster WS, Keller CS, Matsuki M, Clausen TP. 1989. Pollination of Dale- champia magnoliifolia (Euphorbiaceae) by male euglossine bees (Apidae: Euglossini). Am. J. Bot. 76:1279-85
  • Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H. 2002. Compar- ative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae, s.l.). Am. J. Bot. 89:37- 49
  • Armbruster WS, Webster GL. 1982. Diver- gent pollination systems in sympatric species of South American Dalechampia (Euphor- biaceae). Am. Midl. Nat. 108:325-37
  • Baker HG. 1963. Evolutionary mechanisms in pollination biology. Science 139:877-83
  • Baker HG, Baker I. 1983. Floral nectar sugar constituents in relation to pollinator type. In Handbook of Experimental Pollination Bi- ology, ed. CE Jones, RJ Little, pp. 117-41. New York: Van Nostrand Reinhold
  • Baker HG, Baker I. 1990. The predictive value of nectar chemistry to the recognition of pol- linator types. Isr J. Bot. 39:157-66
  • Baum DA, Small RL, Wendel JF. 1998. Bio- geography and floral evolution of baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets. Syst. Biol. 47:181-207
  • Beardsley PM, Yen A, Olmstead RG. 2003. AFLP phylogeny of Mimulus section Ery- thranthe and the evolution of hummingbird pollination. Evolution 57:1397-410
  • Beattie AJ. 1971. Pollination mechanisms in Vi- ola. New Phytol. 70:343-60
  • Berg RL. 1959. A general evolutionary princi- ple underlying the origin of developmental homeostasis. Am. Nat. 93:103-5
  • Berg RL. 1960. The ecological significance of correlation pleiades. Evolution 14:171-80
  • Bingham RA, Orthner AR. 1998. Efficient pol- lination of alpine plants. Nature 391:238-39
  • Bradshaw HD, Schemske DW. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176-78
  • Breedlove DE. 1969. The Systematics of Fuch- sia Section Encliandra (Onagraceae). Berke- ley: Univ. Calif. Press. 69 pp.
  • Bruneau A. 1997. Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae). Am. J. Bot. 84:54-71
  • Buchmann SL. 1987. The ecology of oil flowers and their bees. Annu. Rev. Ecol. Syst. 18:343- 70
  • Campbell DR. 1985. Pollen and gene dispersal: the influence of competition for pollination. Evolution 39:418-31
  • Campbell DR. 1989. Measurements of selec- tion in a hermaphroditic plant: variation in male and female pollination success. Evolu- tion 43:318-34
  • Campbell DR. 1996. Mechanisms of hum- mingbird-mediated selection for flower width in Ipomopsis aggregata. Ecology 77: 1462-72
  • Campbell DR. 1997. Genetic and environ- mental variation in life-history traits of a monocarpic perennial: a decade-long field experiment. Evolution 51:373-82
  • Campbell DR, Waser NM, Meléndez-Acker- man EJ. 1997. Analyzing pollinator-medi- ated selection in a plant hybrid zone: hum- mingbird visitation patterns on three spatial scales. Am. Nat. 149:295-315
  • Campbell DR, Waser NM, Price MV, Lynch EA, Mitchell RJ. 1991. Components of phe- notypic selection: pollen export and flower corolla width in Ipomopsis aggregata. Evo- lution 45:1458-67
  • Cane JH, Eickwort GC, Wesley FR, Spielholz J. 1983. Foraging, grooming and mate-seeking behaviors of Macropsis nuda (Hymenoptera, Melittidae) and use of Lysimachia ciliate (Primulaceae) oils in larval provisions and cell linings. Am. Midl. Nat. 110:257-64
  • Castellanos MC, Wilson P, Thomson JD. 2003. Pollen transfer by hummingbirds and bum- blebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742-52
  • Castellanos MC, Wilson P, Thomson JD. 2004. 'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Pen- stemon flowers. J. Evol. Biol. In press
  • Chase MW, Hills HG. 1992. Orchid phylogeny, flower sexuality, and fragrance-seeking bees. Bioscience 42:43-49
  • Clements FE, Long FL. 1923. Experimental Pollination: An Outline of the Ecology of Flowers and Insects. Publ. 336. Washington, DC: Carnegie Inst. 274 pp.
  • Conner JK, Davis R, Rush S. 1995. The effect of wild radish morphology on pollination ef- ficiency by 4 taxa of pollinators. Oecologia 104:234-45
  • Cresswell JE. 1998. Stabilizing selection and the structural variability of flowers within species. Ann. Bot. 81:463-73
  • Cresswell JE. 2000. Manipulation of female architecture in flowers reveals a narrow optimum for pollen deposition. Ecology 81:3244-49
  • Cresswell JE, Galen C. 1991. Frequency- dependent selection and adaptive surfaces for floral trait combinations: the pollination of Polemonium viscosum. Am. Nat. 138:1342- 53
  • Crisp MD. 1994. Evolution of bird pollination in some Australian legumes (Fabacae). In Phylogenetics and Ecology, ed. P Eggelton, RI Vane-Wright, pp. 281-309. London: Aca- demic
  • Darwin C. 1862. On the Various Contrivances by Which British and Foreign Orchids Are Fertilized. London: Murray. 365 pp.
  • Darwin C. 1877. On the Various Contrivances by Which British and Foreign Orchids Are Fertilized. New York: D. Appleton. 300 pp. 2nd ed.
  • Delpino F. 1868-1875. Ulteriori osservazione sulla dicogamia nel regno vegetale. Atti della Societa Italiana di Scienze Naturali Milano, Vols. 1 and 2
  • Dicks LV, Corbet SA, Pywell RF. 2002. Com- partmentalization in plant-insect flower visi- tor webs. J. Anim. Ecol. 71:32-43
  • Dilley JD, Wilson P, Mesler MR. 2000. The radiation of Calochortus: generalist flowers moving through a mosaic of potential polli- nators. Oikos 89:209-22
  • Dodson CH, Dressler RL, Hills HG, Adams RM, Williams NH. 1969. Biologically ac- tive compounds in orchid fragrances. Science 164:1243-49
  • Dressler RL. 1968. Pollination by male euglos- sine bees. Evolution 22:202-10
  • Dressler RL. 1982. Biology of orchid bees (Euglossini). Annu. Rev. Ecol. Syst. 13:373- 94
  • Fægri K, van der Pijl L. 1966. The Principles of Pollination Ecology. Oxford: Pergamon. 248 PP.
  • Fægri K, van der Pijl L. 1971. The Principles of Pollination Ecology, Oxford: Pergamon. 298 pp. 2nd ed.
  • Fægri K, van der Pijl L. 1979. The Principles of Pollination Ecology, Oxford: Pergamon. 244 pp. 3rd ed.
  • Fenster CB. 1991a. Gene flow in Chamaecrista fasciculata (Leguminosae). I. Gene dispersal Evolution 45:398-409
  • Fenster CB. 199 1b. Selection on floral morphol- ogy by hummingbirds. Biotropica 23:98-101
  • Fenster CB, Dudash MR. 2001. Spatiotempo- ral variation in the role of hummingbirds as pollinators of Silene virginica (Caryophyl- laceae). Ecology 82:844-51
  • Fenster CB, Galloway LF, Chao L. 1997. Epis- tasis and its consequences for the evolution of natural populations. Trends Ecol. Evol. 12: 282-86
  • Fenster CB, Ritland K. 1994. Evidence for nat- ural selection on mating system in Mimu- lus (Scrophulariaceae). Int. J. Plant Sci. 155: 588-96
  • Fishbein M, Venable DL. 1996. Diversity and temporal change in the effective pollina- tors of Asclepias tuberosa. Ecology 77:1061- 73
  • Fleming TH, Holland JN. 1998. The evolution of obligate pollination mutualisms: senita cactus and senita moth. Oecologia 114:368- 75
  • Fulton M, Hodges SA. 1999. Floral isolation between Aquilegia Formosa and Aquilegia pubescens. Proc. R. Soc. London Ser B Biol. Sci. 266:2247-52
  • Futuyma DJ. 1998. Evolutionary Biology. Sun- derland, MA: Sinauer. 810 pp. 3rd ed.
  • Galen C. 1989. Measuring pollinator-mediated selection on morphometric floral traits: bum- ble bees and the alpine skypilot, Polemonium viscosum. Evolution 43:882-90
  • Galen C. 1999. Why do flowers vary? The func- tional ecology of variation in flower size and form within natural plant populations. Bio- science 49:631-40
  • Galen C, Cuba J. 2001. Down the tube: polli- nators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium vis- cosum. Evolution 55:1963-71
  • Goldblatt P, Manning JC. 1996. Phylogeny and speciation in Lapeirousia subgenus Lapeirousia (Iridaceae: Ixioideae). Ann. Mo. Bot. Gard. 83:346-61
  • Goldblatt P, Manning JC, Bernhardt P. 2001. Radiation of pollination systems in Gladiolus (Iridaceae: Crocoideae) in southern Africa. Ann. Mo. Bot. Gard. 88:713-34
  • Gomez JM. 2002. Generalizations in the inter- actions between plants and pollinators. Rev. Chil. Hist. Nat. 75:105-16
  • Gomez JM, Zamora R. 1999. Generalization vs. specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecol- ogy 80:796-805
  • Gould SJ. 1986. Evolution and the triumph of homology, or why history matters. Am. Sci. 74:60-69
  • Grant KA, Grant V. 1968. Hummingbirds and Their Flowers. New York: Columbia Univ. Press. 115 pp.
  • Grant V, Grant KA. 1965. Flower Pollination in the Phlox Family. New York: Columbia Univ. Press. 180 pp.
  • Grant V, Temeles EJ. 1992. Foraging ability of rufous hummingbirds on hummingbird flow- ers and hawkmoth flowers. Proc. Natl. Acad. Sci. USA 89:9400-4
  • Gregory DP. 1963-1964. Hawkmoth pollina- tion in the genus Oenothera. Alisio 5:357- 419
  • Gustaffson L, Sutherland WJ. 1988. The costs of reproduction in the collared flycatchers Ficedula albicollis. Nature 335:813-15
  • Hagerup 0. 1951. Pollination in the faroes- in spite of rain and poverty of insects. Den Konglige Dan. Vidensk. Selskr. Biol. Medd. 18:1-48
  • Hansen T, Armbruster WS, Antonsen L. 2000. Comparative analysis of character displace- ment and spatial adaptations as illustrated by the evolution of Dalechampia blossoms. Am. Nat. 156(Suppl):S17-34
  • Hapeman JR, Inoue K. 1997. Plant-pollinator interaction and floral radiation in Platan- thera (Orchidaceae). In Molecular Evolution and Adaptive Radiation, ed. TJ Givnish, KJ Sytsma, pp. 433-54. Cambridge, UK: Cam- bridge Univ. Press
  • Herre EA, West SA. 1997. Conflict of interest in a mutualism: documenting the elusive fig wasp seed trade-off. Proc. R. Soc. London Ser. B Biol. Sci. 264:1501-7
  • Herrera CM. 1987. Components of pollination "quality": comparative analysis of a diverse insect assemblage. Oikos 50:79-90
  • Herrera CM. 1996. Floral traits and plant adap- tation to insect pollinators: a devil's advocate approach. In Floral Biology: Studies on Flo- ral Evolution in Animal-Pollinated Plants, ed. DG Lloyd, SCH Barrett, pp. 65-87. New York: Chapman & Hall
  • Herrera CM. 2001. Deconstructing a floral phe- notype: Do pollinators select for corolla inte- gration in Lavandula latifolia? J. Evol. Biol. 14:574-84
  • Hodges SA, Arnold ML. 1994. Columbines: a geographically widespread species flock. Proc. Natl. Acad. Sci. USA 91:5129-32
  • Hodges SA, Arnold ML. 1995. Spurring plant diversification: Are floral nectar spurs a key innovation? Proc. R. Soc. London Ser B 262: 343-48
  • Hodges SA, Fulton M, Yang JY, Whittall JB. 2004. Verne Grant and evolutionary studies of Aquilegia. New Phytol. 161:113-20
  • Horvitz CC, Schemske DW. 1990. Spatiotem- poral variation in insect mutualists of a neotropical herb. Ecology 71:1085-97
  • Huang S-Q, Takahashi Y, Dafni A. 2002. Why does the flower stalk of Pulsatilla cernua bend during anthesis? Am. J. Bot. 89:1599- 603
  • Hurlbert AH, Hosoi SA, Temeles EJ, Ewald PW. 1996. Mobility of Impatiens capen- sis flowers: effect on pollen deposition and hummingbird foraging. Oecologia 105:243- 46
  • Inouye DW, Gill DE, Dudash MR, Fenster CB. 1994. A model and lexicon for pollen fate. Am. J. Bot. 81:1517-30
  • Ivey CT, Martinez P, Wyatt R. 2003. Variation in pollinator effectiveness in swamp milkweed, Asclepia incarnata (Apocynaceae). Am. J. Bot. 90:214-25
  • Janzen DH. 1979. How to be a fig. Annu. Rev. Ecol. Syst. 10:13-51
  • Janzen DH. 1980. When is it coevolution? Evo- lution 34:611-12
  • Johnson SD, Linder HP, Steiner KE. 1998. Phy- logeny and radiation of pollination systems in Disa (Orchidaceae). Am. J. Bot. 85:402- 11
  • Johnson SD, Peter CI, Agren J. 2004. The effects of nectar addition on increased pollen removal and geitonogamy in the non- rewarding orchid Anacamptis morio. Proc. Royal Soc. of London Ser B Biol. Sci. 271: 803-9
  • Johnson SD, Steiner KE. 1997. Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchi- daceae). Evolution 51:45-53
  • Johnson SD, Steiner KE. 2000. Generalization vs. specialization in plant pollination sys- tems. Trends Ecol. Evol. 15:140-43
  • Johnston MO. 1991. Natural selection on floral traits in two species of Lobelia with different pollinators. Evolution 45:1468-79
  • Kay KM, Schemske DW. 2003. Pollinator as- semblages and visitation rates for 11 species of Neotropical Costus (Costaceae). Biotrop- ica 35:198-207
  • Kephart S. 1983. The partitioning of pollinators among three species of Asclepias. Ecology 64:120-32
  • Kephart S, Theiss K. 2004. Pollinator-mediated isolation in sympatric milkweeds (Ascle- pias): Do floral morphology and insect be- havior influence species boundaries? New Phytol. 161:263-77
  • Kiester AR, Lande R, Schemske DW. 1984. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124: 220-43
  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vigneri SN, et al. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157:245-61
  • Knuth P. 1906. Handbook of Flower Pollina- tion. Vol. I. Transl. JR Ainsworth Davis. Ox- ford: Clarendon. 382 pp.
  • Knuth P. 1908. Handbook of Flower Pollina- tion. Vol. II. Transl. JR Ainsworth Davis. Ox- ford: Clarendon. 705 pp.
  • Kölreuter JG. 1761. Vorläufige Nachrichten von einigen das Geschlecht der Pflanzen betreffenden Versuchen und Beobachtungen. Leipzig: Gleditschischen Handlung
  • Kurzweil H, Linder HP, Chesselet P. 1991. The phylogeny and evolution of the Pterygodium- Corycium complex (Coryciinae, Orchi- daceae). Plant Syst. Evol. 175:161-223
  • Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. Evolution 37:1210-26
  • Levin DA, Berube DE. 1972. Phlox and Co- lias: the efficiency of a pollination system. Evolution 26:242-50
  • Maad J. 2000. Phenotypic selection in hawk- moth pollinated Platanthera bifolia: tar- gets and fitness surfaces. Evolution 54:112- 23
  • Mayfield MM, Waser NM, Price MV. 2001. Ex- ploring the 'most effective pollinator princi- ple' with complex flowers: bumblebees and Ipomopsis aggregata. Ann. Bot. 88:591-96
  • McDade LA. 1992. Pollinator relationships, biogeography, and phylogenetics. Bio- Science 42:21-26
  • McGall C, Primack RB. 1992. Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am. J. Bot. 79:434-42
  • McGuire AD, Armbruster WS. 1991. An ex- perimental test for the reproductive inter- actions between two sequentially blooming Saxifraga species. Am. J. Bot. 78:214-19
  • Manning JC, Linder HP. 1992. Pollinators and evolution in Disperis (Orchidaceae), or why are there so many species? S. Afr J. Sci. 88: 38-49
  • Medel R, Botto-Mahan C, Kalin-Arroyo M. 2003. Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84:1721-32
  • Meléndez-Ackerman E, Campbell DR. 1998. Adaptive significance of flower color and inter-trait correlations in an Ipomopsis hy- brid zone. Evolution 52:1293-303
  • Meléndez-Ackerman E, Campbell DR, Waser NM. 1997. Hummingbird behavior and mechanisms of selection on flower color in Ipomopsis. Ecology 78:2532-41
  • Mesler MR, Ackerman JD, Lu KL. 1980. The effectiveness of fungus gnats as pollinators. Am J. Bot. 67:564-67
  • Miller RB. 1981. Hawkmoths and the geo- graphic patterns of floral variation in Aqui- legia caerulea. Evolution 35:763-74
  • Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, et al. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant- pollinator community in a lowland diptero- carp forest. Am. J. Bot. 85:1477-501
  • Motten AF, Campbell DR, Alexander DE, Miller HL. 1981. Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62:1278-87
  • Muchhala N. 2003. Exploring the boundary be- tween pollination syndromes: bats and hum- mingbirds as pollinators of Burmeistera cy- clostigmata and B. Tenuiflora (Campanu- laceae). Oecologia 134:373-80
  • Müller H. 1883. The Fertilization of Flow- ers. Transl. D'Arcy W. Thompson. London: Macmillan. 669 pp.
  • Müller H, Delpino F. 1869. Application of the Darwinian theory to flowers and the insects which visit them. Transl. RL Packard. 1871, in Am. Nat. 5:271-97
  • Nilsson LA. 1983. Mimesis of bellflower (Cam- panula) by the red helleborine orchid Cepha- lanthera rubra. Nature 305:799-800
  • Nilsson LA. 1987. Angraecoid orchids and hawkmoths in central Madagascar: special- ized pollination systems and generalist for- agers. Biotropica 19:310-18
  • Nilsson LA. 1988. The evolution of flowers with deep corolla tubes. Nature 334:147-49
  • O'Connell LM, Johnston MO. 1998. Male and female pollination success in a deceptive or- chid, a selection study. Ecology 79:1246- 60
  • Ollerton J. 1996. Reconciling ecological pro- cesses with phylogenetic patterns: the appar- ent paradox of plant-pollinator systems. J. Ecol. 84:767-69
  • Ollerton J. 1998. Sunbird surprise for syn- dromes. Nature 394:726-27
  • Ollerton J, Watts S. 2000. Phenotype space and floral typology--towards an objective assessment of pollination syndromes. Det. Nor. Vidensk. Acad. I. Mat. Natur Ki. Skr. Ny Ser 39:149-59
  • Olsen KM. 1997. Pollination effectiveness and pollinator importance in a population of Het- erotheca subaxillaris (Asteraceae). Oecolo- gia 109:114-21
  • Ornduff R. 1975. Complementary roles of hal- ictids and syrphids in the pollination of Jep- sonia heterandra (Saxifragaceae). Evolution 29:371-73
  • Orr HA. 2000. Adaptation and the cost of com- plexity. Evolution 54:13-20
  • Paige KN, Whitham TG. 1985. Individual and population shifts in flower color by scarlet gilia--a mechanism for pollinator tracking. Science 227:315-17
  • Parker FD. 1981. How efficient are bees in pol- linating sunflowers? J. Kans. Entomol. Soc. 54:61-67
  • Parrish JAD, Bazzaz F. 1979. Differences in pollination niche relationships in early- and late- successional plant communities. Ecol- ogy 60:597-610
  • Patterson TB, Givinish TJ. 2004. Geographic cohesion, chromosomal evolution, parallel adaptive radiations, and consequent flo- ral adaptations in Calochortus (Calochor- taceae): evidence from a cpDNA phylogeny. New Phytol. 161:253-64
  • Peakall R, Handel SN. 1993. Pollinators dis- criminate among floral heights of a sexually deceptive orchid: implications for selection. Evolution 47:1681-87
  • Pellmyr 0. 1986. Three pollination morphs in Cimicifuga simplex: incipient speciation due to inferiority in competition. Oecologia 68:304-7
  • Pellmyr 0. 1997. Pollinating seed eaters: Why is active pollination so rare? Ecology 78:1655-60
  • Pellmyr O, Thompson JN, Brown JM, Harrison RG. 1996. Evolution of pollination and mu- tualism in the yucca moth lineage. Am. Nat. 148:827-47
  • Pettersson MW. 1991. Pollination by a guild of fluctuating moth populations: options for unspecialization in Silene vulgaris. J. Ecol. 79:591-604
  • Pleasants JM. 1980. Competition for bumble- bee pollinators in Rocky Mountain plant communities. Ecology 61:1446-59
  • Pleasants JM. 1990. Null-model tests for com- petitive displacement: the fallacy of not fo- cusing on the whole community. Ecology 71:1078-84
  • Primack RB, Silander JA. 1975. Measuring the relative importance of different pollinators to plants. Nature 255:143-44
  • Pyke GH, Waser NM. 1981. The production of dilute nectars by hummingbird and hon- eyeater flowers. Biotropica 13:260-70
  • Rathcke BJ. 1983. Competition and facilitation among plants for pollination. In Pollination Biology, ed. LA Real, pp. 305-29. New York: Academic
  • Raven PH. 1979. A survey of reproductive bi- ology in Onagraceae. N. Z. J. Bot. 17:575-93
  • Reeves PA, Olmstead RG. 2003. Evolution of the TCP gene family in Asteridae: cladis- tic and network approaches to understanding regulatory gene family diversification and its impact on morphological evolution. Mol. Biol. Evol. 20:1997-2009
  • Robertson C. 1923. Flowers and insects. XXII. Bot. Gaz. 75:60-74
  • Robertson C. 1924. Flowers and insects. XXIII. Bot. Gaz. 78:68-74
  • Robertson C. 1928. Flowers and Insects. Lists of Visitors of Four Hundred and Fifty-Three Flowers. Carlinville, IL: Charles Robertson. 221 pp.
  • Robertson JL, Wyatt R. 1990. Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution 44: 121-33
  • Rush S, Conner JK, Jennetten P. 1995. The ef- fects of natural variation in pollinator visita- tion on rates of pollen removal in wild radish, Raphanus raphanistrum (Brassicaceae). Am. J. Bot. 82:1522-26
  • Schemske DW. 1981. Floral convergence and pollinator sharing in two bee-pollinated trop- ical herbs. Ecology 62:946-54
  • Schemske DW. 1983. Limits to specialization and coevolution in plant-animal mutualisms. In Coevolution, ed. MH Nitecki, pp. 67-110. Chicago: Univ. Chicago Press. 392 pp.
  • Schemske DW, Bradshaw HD. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. USA 96:11910-15
  • Schemske DW, Horvitz CC. 1984. Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225:519-21
  • Schemske DW, Horvitz CC. 1989. Temporal variation in selection on a floral character. Evolution 43:461-65
  • Schemske DW, Lande R. 1984. The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolu- tion 39:41-52
  • Schluter D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-74
  • Simpson BB, Neff JL. 1983. Evolution and di- versity of floral rewards. In Handbook of Experimental Pollination Ecology, ed. CE Jones, RJ Little, pp. 277-93. New York: Van Nostrand Reinhold. 558 pp.
  • Simpson GG. 1944. Tempo and Mode in Evolu- tion. New York: Columbia Univ. Press. 237 pp.
  • Sprengel CK. 1793. Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen. Berlin: Vieweg
  • Sprengel CK. 1996. Discovery of the secret of nature in the structure and fertilization of flowers. In Floral Biology: Studies on Flo- ral Evolution in Animal-Pollinated Plants, ed. DG Lloyd, SCH Barrett, pp. 3-43. Transl. P. Haase. New York: Chapman & Hall. 410 PP.
  • Stebbins GL. 1950. Variation and Evolution In Plants. New York: Columbia Univ. Press. 643 pp.
  • Stebbins GL. 1970. Adaptive radiation of re- productive characteristics in angiosperms. I: Pollination mechanisms. Annu. Rev. Ecol. Syst. 1:307-26
  • Stebbins GL. 1974. Flowering Plants. Evolu- tion Above the Species Level. Cambridge, MA: Harvard Univ. Press. 397 pp.
  • Steiner KE. 1998. The evolution of beetle polli- nation in a South African orchid. Am. J. Bot. 85:1180-93
  • Stone G, Willmer PG, Rowe JA. 1998. Par- titioning of pollinators during flowering in an African Acacia community. Ecology 79:2808-27
  • Sugden EA. 1986. Anthecology and pollination efficacy of Styrax officinale subsp. redivivum (Styracaceae). Am. J. Bot. 73:919-30
  • Tanaka N, Setoguchi H, Murata J. 1997. Phy- logeny of the family Hydrocharitaceae in- ferred from rbcL and matK gene sequence data. J. Plant Res. 110:329-37
  • Tandon R, Shivanna KR, Mohan Ram HY. 2003. Reproductive biology of Butea mono- sperma (Fabaceae). Ann. Bot. 92:715-28
  • Temeles EJ. 1996. A new dimension to hum- mingbird-flower relationships. Oecologia 105:517-23
  • Temeles EJ, Kress WJ. 2003. Adaptation in a plant-hummingbird association. Science 300:630-33
  • Temeles EJ, Linhart YB, Masonjones M, Ma- sonjones HD. 2002. The role of flower width in hummingbird bill length-flower length re- lationships. Biotropica 34:68-80
  • Temeles EJ, Rankin AG. 2000. Effect of the lower lip of Monarda didyma on pollen re- moval by hummingbirds. Can. J. Bot. 78: 1164-68
  • Thompson JN. 1994. The Coevolutionary Pro- cess. Chicago: Univ. Chicago Press. 376 pp.
  • Thompson JN. 1999. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153(Suppl.):S1-14
  • Thomson BA, Thomson JD. 1998. BeeVisit for Windows (Visual Basic interactive simula- tion package for pollination). In BioQUEST Library Vol. V The BioQUEST Curriculum Consortium. New York: Academic
  • Thomson JD. 2003. When is it mutualism? 2001 Presidential Address, American Society of Naturalists. Am. Nat. 162:S1-9
  • Thomson JD, Thomson BA. 1992. Pollen pre- sentation and viability schedules in animal- pollinated plants: consequences for repro- ductive success. In Ecology and Evolution of Plant Reproduction: New Approaches, ed. R. Wyatt, pp. 1-24. New York: Chapman & Hall
  • Thomson JD, Wilson P, Valenzuela M, Malzone M. 2000. Pollen presentation and pollination syndromes, with special reference to Penste- mon. Plant Species Biol. 15:11-29
  • Totland 0. 2001. Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233-44
  • Walker-Larson J, Harder LD. 2001. Vestigial organs as opportunities for functional inno- vation: the example of the Penstemon stamin- ode. Evolution 55:477-87
  • Waser NM. 1988. Comparative pollen and dye transfer by pollinators of Delphinium nel- sonii. Funct. Ecol. 2:41-48
  • Waser NM. 1998. Pollination, angiosperm spe- ciation, and the nature of species boundaries. Oikos 81:198-201
  • Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. 1996. Generalization in pollina- tion systems, and why it matters. Ecology 77:1043-60
  • Waser NM, Price MV. 1981. Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution 35:376-90
  • Waser NM, Price MV. 1983. Pollinator behav- ior and natural selection for flower color in Delphinium nelsonii. Nature 302:422-24
  • Waser NM, Price MV. 1998. What plant ecolo- gists can learn from zoology. Perspect. Plant Ecol. Evol. Syst. 1:137-50
  • Weiblen GD. 2002. How to be a fig wasp. Annu. Rev. Entomol. 47:299-330
  • Weller SG, Sakai AK, Rankin AE, Golonka A, Kutcher B, Ashby KE. 1998. Dioecy and the evolution of pollination systems in Schiedea and Alsinidendron (Caryophyllaceae: Alsi- noideae) in the Hawaiian Islands. Am. J. Bot. 85:1377-88
  • Wesselingh RA, Arnold ML. 2000. Pollinator behaviour and the evolution of Louisiana iris hybrid zones. J. Evol. Biol. 13:171-80
  • Whalen MD. 1978. Reproductive character dis- placement and floral diversity in Solanum section Androceras. Syst. Bot. 3:77-86
  • Whitten WM, Hills HG, Williams NH. 1998. Occurrence of ipsdienol in floral fragrances. Phytochemistry 27:2759-60
  • Wiebes JT. 1979. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10:1-12
  • Williams GC. 1992. Natural Selection: Do- mains, Levels, and Challenges. Oxford: Ox- ford Univ. Press. 208 pp.
  • Wilson P. 1995. Selection for pollination suc- cess and the mechanical fit of Impatiens flow- ers around bumblebee bodies. Biol. J. Linn. Soc. 55:355-83
  • Wilson P, Castellanos MC, Hogue JN, Thom- son JD, Armbruster WS. 2004. A multivari- ate search for pollination syndromes among penstemons. Oikos 104:345-61
  • Wilson P, Castellanos MC, Wolfe A, Thom- son JD. 2004. Shifts between bee- and bird- pollination among penstemons. In Speciali- zation and Generalization in Plant-Polli- nator Interactions, ed. N. Waser, J. Ollerton. Chicago: Univ. Chicago Press. In press
  • Wilson P, Thomson JD. 1996. How do flowers diverge? In Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants, ed. DG Lloyd, SCH Barrett, pp. 88-111. New York: Chapman & Hall
  • Wolfe LM, Barrett SCH. 1988. Temporal changes in the pollinator fauna of tristylous Pontederia-cordata, an aquatic plant. Can. J. Zool. 66:1421-24
  • Wolfe LM, Kristolic JL. 1999. Floral symmetry and its influence on variance in flower size. Am. Nat. 154:484-88
  • Wright S. 1931. Evolution in mendelian popu- lations. Genetics 16:97-59