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Associations between floral specialization and species diversity: cause, effect, or correlation?

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Abstract

It has been proposed frequently, from Darwin’s time onwards, that specialized pollination increases speciation rates and thus the diversity of plant species (i.e. clade species richness). We suggest here that the correlation between clade species richness and floral specialization is real, but that clade species richness is frequently the cause, not the result of floral specialization. We urge a broader, variance-partitioning perspective for assessing the causes of this correlation by suggesting four models of how the diversity-specialization correlation might come about: (1) floral specialization promotes initial reproductive isolation (“Initial-RI” model), (2) floral specialization promotes reinforcement of reproductive isolation upon secondary contact (“Reinforcement” model), (3) floral specialization reduces the extinction rate by promoting tighter species packing (“Extinction” model), (4) floral specialization is the result of high clade species richness, which increases the number of related species in communities, and thus selects for floral character displacement (“Character-Displacement” model). These hypotheses are evaluated by comparing the relationships between species richness, speciation mechanisms, and pollination precision, accuracy, and specialization in the broader literature and, more specifically, in four study systems: Dalechampia (Euphorbiaceae), Collinsia (Plantaginaceae), Burmeistera (Campanulaceae), and Stylidium (Stylidiaceae). These systems provide stronger support for the character-displacement hypothesis, wherein local species diversity drives the evolution of specialized pollination. Although the two reproductive-isolation hypotheses may hold for plants like orchids, with extremely precise pollination systems, the reproductive character-displacement hypothesis seems likely to be more important for plant groups with less precise pollination systems.

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References

  • Aldridge G, Campbell DR (2007) Variation in pollinator preference between two Ipomopsis contact sites that differ in hybridization rate. Evolution 61:99–110

    PubMed  Google Scholar 

  • Armbruster WS (1985) Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution 39:733–752

    Google Scholar 

  • Armbruster WS (1986) Reproductive interactions between sympatric Dalechampia species: are natural assemblages "random" or organized? Ecology 67:522–533

    Google Scholar 

  • Armbruster WS (1988) Multilevel comparative analysis of morphology, function, and evolution of Dalechampia blossoms. Ecology 69:1746–1761

    Google Scholar 

  • Armbruster WS (1990) Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. Am Nat 135:14–31

    Google Scholar 

  • Armbruster WS (1993) Evolution of plant pollination systems: hypotheses and tests with the neotropical vine Dalechampia. Evolution 47:1480–1505

    Google Scholar 

  • Armbruster WS (1997) Exaptations link the evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78:1661–1674

    Google Scholar 

  • Armbruster WS (2006) Evolutionary and ecological perspectives on specialization: from the arctic to the tropics. In: Waser N, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 260–282

    Google Scholar 

  • Armbruster WS, Herzig AL (1984) Partitioning and sharing of pollinators by four sympatric species of Dalechampia (Euphorbiaceae) in Panama. Ann Missouri Botanical Garden 71:1–16

    Google Scholar 

  • Armbruster WS, Steiner KE (1992) Pollination ecology of four Dalechampia species (Euphorbiaceae) in northern Natal, South Africa. Am J Bot 79:306–313

    Google Scholar 

  • Armbruster WS, Webster GL (1982) Divergent pollination systems in sympatric species of South American Dalechampia (Euphorbiaceae). Am Midl Nat 108:325–337

    Google Scholar 

  • Armbruster WS, Herzig AL, Clausen TP (1992) Pollination of two sympatric species of Dalechampia (Euphorbiaceae) in Suriname by male euglossine bees. Amer J Bot 79:1374–1381

    Google Scholar 

  • Armbruster WS, Edwards ME, Debevec EM (1994) Character displacement generates assemblage structure of Western Australian triggerplants (Stylidium). Ecology 75:315–329

    Google Scholar 

  • 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 reevaluation of Berg’s correlation-pleiades concept. Am J Bot 86:39–55

    Google Scholar 

  • Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae, s.l.). Amer J Bot 89:37–49

    Google Scholar 

  • Armbruster WS, Pélabon C, Hansen TF, Mulder CPH (2004) Floral integration and modularity: distinguishing complex adaptations from genetic constraints. In: Pigliucci M, Preston KA (eds) The evolutionary biology of complex phenotypes, Oxford University Press, Oxford, pp 23–49

    Google Scholar 

  • Berg RL (1960) The ecological significance of correlation pleiades. Evolution 14:171–180

    Google Scholar 

  • Bolmgren K, Eriksson O, Linder HP (2003) Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms. Evolution 57:2001–2011

    PubMed  Google Scholar 

  • Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178

    PubMed  CAS  Google Scholar 

  • Brown JH, Kodric-Brown A (1979) Convergence, competition, and mimicry in a temperate community of hummingbird-pollinated flowers. Ecology 60:1022–1035

    Google Scholar 

  • Butlin R (1989) Reinforcement of premating isolation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer, Sunderland, MA, pp 158–179

    Google Scholar 

  • Chase MW, Hills HG (1992) Orchid phylogeny, flower sexuality, and fragrance-seeking bees. BioScience 42:43–49

    Google Scholar 

  • Coates DJ, Carstairs S, Hamley VL (2003) Evolutionary patterns and genetic structure in localized and widespread species in the Stylidium caricifolium complex (Stylidiaceae). Am J Bot 90:997–1008

    CAS  Google Scholar 

  • Cooley AM, Carvallo G, Willis JH (2008) Is floral diversification associated with ollinator divergence? Flower shape, flower colour and pollinator preferencein Chilean Mimulus. Ann Bot 101:641–650

    PubMed  CAS  Google Scholar 

  • Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trend Ecol Evol 20:487–494

    Google Scholar 

  • Cozzolino S, Scopece G (2008) Deceptive orchids: the promise of sex or food and its consequences for reproductive isolation. Phil Trans R Soc B (in press)

  • Cozzolino S, Schiestl FP, Muller A, De Castro O, Nardella AM, Widmer A (2005) Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: absence of premating barriers? Proc R Soc B Biol Sci 272:1271–1278

    Google Scholar 

  • Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381

    Google Scholar 

  • Crepet WL (1984) Advanced (constant) insect pollination mechanisms—pattern of evolution and implications vis-a-vis angiosperm diversity. Ann Miss Bot Gard 71:607–630

    Google Scholar 

  • Cronquist A (1982) An integrated system of classification of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Darwin C (1876) The effects of cross—and self-fertilization in the vegetable kingdom. John Murray, London

    Google Scholar 

  • Darwin C (1877) The various contrivances by which orchids are fertilised by insects. Republished 1984, University of Chicago Press, Chicago

  • Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin’s abominable mystery: Insights from a supertree of the angiosperms. Proc Nat Acad Sci USA 101:1904–1909

    PubMed  CAS  Google Scholar 

  • Diggle PK (1992) Development and the evolution of plant reproductive characters. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman & Hall, New York, pp 326–355

    Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia Univ Press, New York

    Google Scholar 

  • Dodd ME, Silvertown J, Chase MW (2000) Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53:732–744

    Google Scholar 

  • Dodson CH (1962) The importance of pollinators in the evolution of the orchids of tropical America. Am Orchid Soc Bull 31:525–534, 641–649, 731–735

    Google Scholar 

  • Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210

    Google Scholar 

  • Dressler RL (1981) The orchids: natural history and classification. Harvard University Press, Cambridge, Mass, USA

    Google Scholar 

  • Ennos RA (2008) Spurred by pollinators. Heredity 100:3–4

    PubMed  CAS  Google Scholar 

  • Fægri K, van der Pijl L (1979) The principles of pollination ecology, 3rd edn. Pergamon, Oxford, 244 pp

    Google Scholar 

  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JT (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403

    Google Scholar 

  • Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733

    Google Scholar 

  • Gegear RJ, Burns JG (2007) The birds, the bees, and the virtual flowers: can pollinator behavior drive ecological speciation in flowering plants? American Naturalist 170:551–566

    PubMed  Google Scholar 

  • Goldblatt P, Manning JC, Bernhardt P (1995) Pollination biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in Southern Africa––floral divergence and adaptation for long-tongued fly pollination. Ann Mis Bot Gard 82:517–534

    Google Scholar 

  • Grant V (1949) Pollination systems as isolating mechanisms in plants. Evolution 3:82–97

    PubMed  CAS  Google Scholar 

  • Grant V (1966) The selective origin of incompatibility barriers in the plant genus Gilia. Am Nat 100:99–118

    Google Scholar 

  • Grant V (1971) Plant speciation, 2nd edn. Columbia University Press, New York, NY, USA

    Google Scholar 

  • Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proc Nat Acad Sci USA 91:3–10

    PubMed  CAS  Google Scholar 

  • Grant V, Grant KA (1965) Pollination in the phlox family. Columbia University Press, New York

    Google Scholar 

  • Hansen TF, Carter AJR, Pélabon C (2006) On adaptive accuracy and precision in natural populations. Am Nat 168:168–181

    PubMed  Google Scholar 

  • Heinrich B. Raven PH (1972) Energetics and pollination ecology. Science 176:597–602

    Google Scholar 

  • Hersch EI, Roy BA (2007) Context-dependent pollinator behavior: an explanation for patterns of hybridization among three species of Indian paintbrush. Evolution 61:111–124

    PubMed  Google Scholar 

  • Hodges SA (1997) Floral nectar spurs and diversification. Int J Plant Sci 158:S81–S88

    Google Scholar 

  • Hodges SA, Arnold ML (1995) Spurring plant diversification: are floral nectar spurs a key innovation? Proc R Soc Lond B Biol Sci 262:343–348

    Google Scholar 

  • Hodges SA, Whittall JB (2008) One-sided evolution or two? A reply to ennos. Heredity (advance online publication) doi:10.1038/hdy.2008.12

  • Hopper SD (1979) Biogeographical aspects of speciation in the southwest Australian flora. Annu Rev Ecol Syst 10:399–422

    Google Scholar 

  • Hoskin J, Higgie M, McDonald KR, Moritz C (2005) Reinforcement drives rapid allopatric speciation. Nature 437:1353–1356

    PubMed  CAS  Google Scholar 

  • Howell DJ (1977) Time sharing and body partitioning in bat-plant pollination systems. Nature 270:509–510

    Google Scholar 

  • Inoue K, Amano M (1986) Evolution of Campanula punctata Lam. in the Izu Islands: changes of pollinators and evolution of breeding systems. Plant Spec Biol 1:89–97

    Google Scholar 

  • Jesson LK (2007) Ecological correlates of diversification in New Zealand angiosperm lineages. N Z J Bot 45:35–51

    Google Scholar 

  • Johnson SD (2007) Pollinator-driven speciation in plants. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, UK, pp 295–310

    Google Scholar 

  • Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51:45–53

    Google Scholar 

  • Keller CS, Armbruster WS (1989) Pollination of Hyptis capitata in Panama by eumenid wasps. Biotropica 21:190–192

    Google Scholar 

  • Knox EB, Muasya AM, Muchhala N (2008) The predominantly South American clade of Lobeliaceae. Sys Bot (in press)

  • Kozak KH, Larson AA, Bonett RM, Harmon LJ (2005) Phylogenetic analysis of ecomorphological divergence, community structure, and diversification rates in dusky salamanders (Plethodontidae: Desmognathus). Evolution 9:2000–2016

    Google Scholar 

  • Lukhtanov VA, Kandul NP, Plotkin JB, Dantchenko AV, Haig D, Pierce NE (2005) Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature 436:385–389

    PubMed  CAS  Google Scholar 

  • Macior LW (1975) The pollination ecology of Pedicularis (Scrophulariaceae) in the Yukon Territory. Am J Bot 62:1065–1072

    Google Scholar 

  • Macior LW (1983) The pollination dynamics of sympatric species of Pedicularis (Scrophulariaceae). Am J Bot 70:844–853

    Google Scholar 

  • McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology’s role in speciation. Nature 429:294–298

    PubMed  CAS  Google Scholar 

  • Miller RB (1981) Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution 35:763–774

    Google Scholar 

  • Miyake T, Inoue K (2003) Character displacement in style length between pollinator-sharing Clerodendrum trichotomum and C. izuinsulare (Verbenaceae). Plant Syst Evol 243:31–38

    Google Scholar 

  • Moyle LC, Olson MS, Tiffin P (2004) Patterns of reproductive isolation in three angiosperm genera. Evolution 58:1195–1208

    PubMed  Google Scholar 

  • Muchhala N (2003) Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae). Oecologia 134:373–380

    PubMed  Google Scholar 

  • Muchhala N (2006a) The pollination biology of Burmeistera (Campanulaceae): specialization and syndromes. Am J Bot 93:1081–1089

    Google Scholar 

  • Muchhala N (2006b) Nectar bat stows huge tongue in its rib cage. Nature 444:701–702

    PubMed  CAS  Google Scholar 

  • Muchhala N (2007) Adaptive tradeoff in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds. Am Nat 169:494–504

    PubMed  Google Scholar 

  • Muchhala N (2008) Functional significance of interspecific variation in Burmeistera flower morphology: evidence from bat captures. Biotropica doi:10.1111/j.1744-7429.2007.00381.x

  • Muchhala N, Potts MD (2007) Character displacement among bat-pollinated flowers of the genus Burmeistera: analysis of mechanism, process, and pattern. Proc R Soc B 274:2731–2737

    Google Scholar 

  • Murcia C, Feinsinger P (1996) Interspecific pollen loss by hummingbirds visiting flower mixtures: effects of floral architecture. Ecology 77:550–560

    Google Scholar 

  • Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149

    Google Scholar 

  • Nilsson LA, Jonsson L, Ralison L, Randrianjohany E (1987) Angrecoid orchids and hawkmoths in central Madagascar: specialized pollination systems and generalist foragers. Biotropica 19:310–318

    Google Scholar 

  • Noor MAF. 1999. Reinforcement and other consequences of sympatry. Heredity 83:503–508

    PubMed  Google Scholar 

  • Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant-pollinator systems. J Ecol 84:767–769

    Google Scholar 

  • Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56:717–728

    Google Scholar 

  • Orr HA (2005) The genetic basis of reproductive isolation: insights from Drosophila. Proc Nat Acad Sci USA 102:6522–6526

    PubMed  CAS  Google Scholar 

  • Pauw A (2006) Floral syndromes accurately predict pollination by a specialized oil-collecting bee (Rediviva peringueyi, Melittidae) in a guild of South African orchids (Coryciinae). Am J Bot 93:917–926

    Google Scholar 

  • Pélabon C, Carlson ML, Hansen TF, Armbruster WS (2004) Variational and genetic properties of developmental stability in Dalechampia scandens. Evolution 58:504–514

    PubMed  Google Scholar 

  • Pélabon C, Carlson ML, Hansen TF, Armbruster WS (2005) Effects of crossing distance on offspring fitness and developmental stability in Dalechampia scandens (Euphorbiaceae). Am J Bot 92:842–851

    Google Scholar 

  • Pellmyr O (1986) Three pollination morphs in Cimicifuga simplex—Incipient speciation due to inferiority in competition. Oecologia 68:304–307

    Google Scholar 

  • Perret M, Chautems A, Spichiger R, Barraclough TG, Savolainen V (2007) The geographical pattern of speciation and floral diversification in the neotropics: the tribe Sinningieae (Gesneriaceae) as a case study. Evolution 61:1641–1660

    PubMed  Google Scholar 

  • Raven PH (1977) A suggestion concerning the cretaceous rise to dominance of the angiosperms. Evolution 31(2):451–452

    Google Scholar 

  • Regal PJ (1977) Ecology and evolution of flowering plant dominance. Science 196:622–629

    PubMed  Google Scholar 

  • Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637–1653

    Google Scholar 

  • Ricklefs RE, Renner SS (1994) Species richness within families of flowering plants. Evolution 48:1619–1636

    Google Scholar 

  • Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914

    PubMed  CAS  Google Scholar 

  • Rieseberg LH, Church SA, Morjan CL (2004) Integration of populations and differentiation of species. New Phytol 161:59–69

    PubMed  CAS  Google Scholar 

  • Robertson JL, Wyatt R (1990) Evidence for pollination ecotypes in the yellow-fringed orchid, Platanthera ciliaris. Evolution 44:121–33

    Google Scholar 

  • Roughgarden J (1979) Theory of population genetics and evolutionary ecology: an introduction. MacMillan, New York, 612 pp

    Google Scholar 

  • Sargent RD (2004) Floral symmetry affects speciation rates in angiosperms. Proc R Soc Lond B Biol Sci 271:603–608

    Google Scholar 

  • Schemske DW, Bradshaw HD (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Nat Acad Sci USA 96:11910–11915

    Google Scholar 

  • Scopece G, Musacchio A, Widmer A, Cozzolino S (2007) Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61:2623–2642

    PubMed  Google Scholar 

  • Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Ann Rev Ecol Syst 34:339–364

    Google Scholar 

  • Smith SA, Rausher MD (2007) Experimental evidence that selection favors character displacement in the ivyleaf morning glory. Am Nat 171:1–9

    Google Scholar 

  • Smith SA, Montes de Oca AN, Reeder TW, Wiens JJ (2007) A phylogenetic perspective on elevational species richness patterns in Middle American treefrogs: why so few species in lowland tropical rainforests? Evolution 61:1188–1207

    PubMed  Google Scholar 

  • Smith CI, Pellmyr O, Althoff DM, Balcazar-Lara M, Leebens-Mack J, Segraves KA (2008) Pattern and timing of diversification in Yucca (Agavaceae): specialized pollination does not escalate rates of diversification. Proc R Soc B Biol Sci 275:249–258

    Google Scholar 

  • Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination mechanisms. Ann Rev Ecol Syst 1:307–326

    Google Scholar 

  • Stebbins GL (1974) Plant species. Evolution above the species level. Harvard University Press, Cambridge, Massachusetts, USA

    Google Scholar 

  • Steiner KE, Whitehead VB (1988) The association between oil-collecting flowers and oil-collecting bees in the Drakensberg of southern Africa. Monograph Syst Bot Mis Bot Gard 25:259–277

    Google Scholar 

  • Steiner KE, Whitehead VB (1990) Pollinator adaptation to oil-secreting flowers – Rediviva and Diascia. Evolution 44:1701–1707

    Google Scholar 

  • Steiner KE, Whitehead VB (1991) Oil flowers and oil bees: further evidence for pollinator adaptation. Evolution 45:1493–1501

    Google Scholar 

  • Stone GN, Willmer P, Rowe JA (1998) Partitioning of pollinators during flowering in an African Acacia community. Ecology 79:2808–2827

    Google Scholar 

  • Straw RM (1955) Hybridization, homogamy, and sympatric speciation. Evolution 9:441–444

    Google Scholar 

  • Straw RM (1956) Floral isolation in Penstemon. Am Nat 90:47–53

    Google Scholar 

  • Susuki K (1992) Bumblebee pollinators and pollination ecotypes of Isodon umbrosus and I. shikokianus (Lamiaceae). Plant Spec Biol 7:37–48

    Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago, USA

    Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolutionary. University of Chicago Press, Chicago, USA

    Google Scholar 

  • Tschapka MS, Dressler S, van Helversen O (2006) Bat visits to Marcgravia pittieri and notes on the inflorescence diversity within the genus Marcgravia (Marcgraviaceae). Flora 201:383–388

    Google Scholar 

  • van der Niet TS, Johnson SD, Linder HP (2006) Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60:1596–1601

    Article  PubMed  Google Scholar 

  • Verdu M (2002) Age at maturity and diversification in woody angiosperms. Evolution 56:1352–1361

    PubMed  Google Scholar 

  • Waser NM (1983) Competition for pollination and floral character differences among sympatric plant species: a review of the evidence. In: Jones CE, Little RJ (eds) Handbook of experimental pollination ecology. Van Nostrand Reinhold, New York, pp 277–293

    Google Scholar 

  • Waser NM (1998) Pollination, angiosperm speciation, and the nature of species boundaries. Oikos 82:198–201

    Google Scholar 

  • Waser NM (2001) Pollinator behavior and plant speciation: looking beyond the “ethological isolation” paradigm. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination Cambridge University Press, Cambridge, UK, pp 318–335

    Google Scholar 

  • Waser NM, Campbell DR (2004) Ecological speciation in flowering plants. In: Dieckmann U, Doebeli M, Metz JAJ, Tautz D (eds) Adaptive speciation. Cambridge University Press, Cambridge, UK, pp 264–277

    Google Scholar 

  • Waser NM, Chittka L, Price M, Williams N, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Google Scholar 

  • Wasserthal LT (1997) The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift. Botanica Acta 110:343–359

    Google Scholar 

  • Wege J (1999) Morphological and anatomical variation within Stylidium (Stylidiaceae)––a systematic perspective. PhD Thesis, University of Western Australia, Perth

  • Whalen MD (1978) Reproductive character displacement and floral diversity in Solanum sect. Androceras. Syst Bot 3:77–86

    Google Scholar 

  • Whittall JB, Hodges SA (2007). Pollination shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–709

    PubMed  CAS  Google Scholar 

  • Wright S (1940) Breeding structure of populations in relation to speciation. Am Nat 74:232–48

    Google Scholar 

  • Yang CF, Gituru RW, Guo YH (2007) Reproductive isolation of two sympatric louseworts, Pedicularis rhinanthoides and Pedicularis longiflora (Orobanchaceae): how does the same pollinator type avoid interspecific pollen transfer? Biol J Linnean Soc 90:37–48

    Google Scholar 

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Acknowledgments

We thank numerous students, postdoctoral researchers, and collaborators for stimulating discussions and help in the field and glasshouse collecting the morphological and pollination data used in this paper. We thank Roger Härdling, Kathleen Donohue, and two anonymous reviewers for comments on an earlier draft of this paper. Research was funded by the US National Science Foundation (DEB−0324808, DEB-0444745) and the Norwegian Research Council.

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  1. School of Biological Sciences, University of Portsmouth, Portsmouth, PO1 2DY, UK

    W. Scott Armbruster

  2. Institute of Arctic Biology, University of Alaska, Fairbanks, AK, 99775-7000, USA

    W. Scott Armbruster

  3. Department of Biology, Norwegian University of Science & Technology, Trondheim, 7491, Norway

    W. Scott Armbruster

  4. Department of Ecology and Evolution, University of Toronto, Toronto, ON, Canada, M5S 3G5

    Nathan Muchhala

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Armbruster, W.S., Muchhala, N. Associations between floral specialization and species diversity: cause, effect, or correlation?. Evol Ecol 23, 159–179 (2009). https://doi.org/10.1007/s10682-008-9259-z

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