1932

Abstract

Understanding how pollen moves between species is critical to understanding speciation, diversification, and evolution of flowering plants. For co-flowering species that share pollinators, competition through interspecific pollen transfer (IPT) can profoundly impact floral evolution, decreasing female fitness via heterospecific pollen deposition on stigmas and male fitness via pollen misplacement during visits to heterospecific flowers. The pollination literature demonstrates that such reproductive interference frequently selects for reproductive character displacement in floral traits linked to pollinator attraction, pollen placement, and mating systems and has also revealed that IPT between given pairs of species is typically asymmetric. More recent work is starting to elucidate its importance to the speciation process, clarifying the link between IPT and current and historical patterns of hybridization, the evolution of phenotypic novelty through adaptive introgression, and the rise of reproductive isolation. Our review aims to stimulate further research on IPT as a ubiquitous mechanism that plays a central role in angiosperm diversification.

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2019-11-02
2024-05-20
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Literature Cited

  1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE et al. 2013. Hybridization and speciation. J. Evol. Biol. 26:229–46
    [Google Scholar]
  2. Alarcon R, Campbell DR. 2000. Absence of conspecific pollen advantage in the dynamics of an Ipomopsis (Polemoniaceae) hybrid zone. Am. J. Bot. 87:6819–24
    [Google Scholar]
  3. Albrecht M, Ramis MR, Traveset A 2016. Pollinator-mediated impacts of alien invasive plants on the pollination of native plants: the role of spatial scale and distinct behaviour among pollinator guilds. Biol. Invasions 18:71801–12
    [Google Scholar]
  4. Aldridge G, Campbell DR. 2006. Asymmetrical pollen success in Ipomopsis (Polemoniaceae) contact sites. Am. J. Bot. 93:903–9
    [Google Scholar]
  5. Aldridge G, Campbell DR. 2007. Variation in pollinator preference between two Ipomopsis contact sites that differ in hybridization rate. Evolution 61:99–110
    [Google Scholar]
  6. Amaya-Márquez M. 2009. Floral constancy in bees: a revision of theories and a comparison with other pollinators. Rev. Colomb. Entomol. 35:206–16
    [Google Scholar]
  7. Anderson B, Alexandersson R, Johnson SD 2010. Evolution and coexistence of pollination ecotypes in an African Gladiolus (Iridaceae). Evolution 64:4960–72
    [Google Scholar]
  8. Anderson B, Pauw A, Cole WW, Barrett SCH 2016. Pollination, mating and reproductive fitness in a plant population with bimodal floral-tube length. J. Evol. Biol. 29:1631–42
    [Google Scholar]
  9. Andrew RL, Kane NC, Baute GJ, Grassa CJ, Rieseberg LH 2013. Recent nonhybrid origin of sunflower ecotypes in a novel habitat. Mol. Ecol. 22:799–813
    [Google Scholar]
  10. Andrew RL, Ostevik KL, Ebert DP, Rieseberg LH 2012. Adaptation with gene flow across the landscape in a dune sunflower. Mol. Ecol. 21:2078–91
    [Google Scholar]
  11. Arceo-Gómez G, Abdala-Roberts L, Jankowiak A, Kohler C, Meindl GA et al. 2016a. Patterns of among- and within-species variation in heterospecific pollen receipt: the importance of ecological generalization. Am. J. Bot. 103:3396–407
    [Google Scholar]
  12. Arceo-Gómez G, Alonso C, Ashman TL, Parra-Tabla V 2018. Variation in sampling effort affects the observed richness of plant–plant interactions via heterospecific pollen transfer: implications for interpretation of pollen transfer networks. Am. J. Bot. 105:91601–8
    [Google Scholar]
  13. Arceo-Gómez G, Ashman TL. 2011. Heterospecific pollen deposition: Does diversity alter the consequences. New Phytol 192:3738–46
    [Google Scholar]
  14. Arceo-Gómez G, Ashman T-L. 2014. Coflowering community context influences female fitness and alters the adaptive value of flower longevity in Mimulus guttatus. Am. Nat 183:2E50–63
    [Google Scholar]
  15. Arceo-Gómez G, Raguso RA, Geber MA 2016b. Can plants evolve tolerance mechanisms to heterospecific pollen effects? An experimental test of the adaptive potential in Clarkia species. Oikos 125:5718–25
    [Google Scholar]
  16. Armbruster WS. 2014. Floral specialization and angiosperm diversity: phenotypic divergence, fitness trade-offs and realized pollination accuracy. AoB PLANTS 6:Sept.plu003
    [Google Scholar]
  17. Armbruster WS, Edwards ME, Debevec EM 1994. Floral character displacement generates assemblage structure of Western Australian triggerplants (Stylidium). Ecology 75:2315–29
    [Google Scholar]
  18. Armbruster WS, Hansen TF, Pélabon C, Pérez-Barrales R, Maad J 2009. The adaptive accuracy of flowers: measurement and microevolutionary patterns. Ann. Bot. 103:91529–45
    [Google Scholar]
  19. Armbruster WS, Shi XQ, Huang S-Q 2014. Do specialized flowers promote reproductive isolation? Realized pollination accuracy of three sympatric Pedicularis species. Ann. Bot. 113:2331–40
    [Google Scholar]
  20. Arnold ML, Cornman RS, Martin NH 2008. Hybridization, hybrid fitness and the evolution of adaptations. Plant Biosyst 142:1166–71
    [Google Scholar]
  21. Arnold ML, Hamrick JL, Bennett BD 1993. Interspecific pollen competition and reproductive isolation in Iris. J. Hered 84:13–16
    [Google Scholar]
  22. Arnold ML, Tang S, Knapp SJ, Martin NH 2010. Asymmetric introgressive hybridization among Louisiana iris species. Genes 1:9–22
    [Google Scholar]
  23. Ashman TL, Arceo-Gómez G. 2013. Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am. J. Bot. 100:61061–70
    [Google Scholar]
  24. Baack E, Melo MC, Rieseberg LH, Ortiz-Barrientos D 2015. The origins of reproductive isolation in plants. New Phytol 207:968–84
    [Google Scholar]
  25. Barrett SCH, Harder LD. 2017. The ecology of mating and its evolutionary consequences in seed plants. Annu. Rev. Ecol. Evol. Syst. 48:135–57
    [Google Scholar]
  26. Bascompte J, Jordano P, Olesen JM 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:April431–33
    [Google Scholar]
  27. Beans CM. 2014. The case for character displacement in plants. Ecol. Evol. 4:6852–65
    [Google Scholar]
  28. Bedinger PA, Broz AK, Tovar-Mendez A, McClure B 2017. Pollen-pistil interactions and their role in mate selection. Plant Physiol 173:179–90
    [Google Scholar]
  29. Bell JM, Karron JD, Mitchell RJ 2005. Interspecific competition for pollination lowers seed production and outcrossing in Mimulus ringens. Am. J. Bot 86:3762–71
    [Google Scholar]
  30. Borchsenius F, Lozada T, Knudsen JT 2016. Reproductive isolation of sympatric forms of the understorey palm Geonoma macrostachys in western Amazonia. Bot. J. Linn. Soc. 182:2398–410
    [Google Scholar]
  31. Brandvain Y, Haig D. 2005. Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. Am. Nat. 166:3330–38
    [Google Scholar]
  32. Briggs HM, Anderson LM, Atalla LM, Delva AM, Dobbs EK, Brosi BJ 2015. Heterospecific pollen deposition in Delphinium barbeyi: linking stigmatic pollen loads to reproductive output in the field. Ann. Bot. 117:341–47
    [Google Scholar]
  33. Briscoe Runquist RD. 2012. Pollinator-mediated competition between two congeners, Limnanthes douglasii subsp. rosea and L. alba (Limnanthaceae). Am. J. Bot. 99:71125–32
    [Google Scholar]
  34. Briscoe Runquist RD, Chu E, Iverson JL, Kopp JC, Moeller DA 2014. Rapid evolution of reproductive isolation between incipient outcrossing and selfing Clarkia species. Evolution 68:102885–900
    [Google Scholar]
  35. Briscoe Runquist RD, Moeller DA 2014. Floral and mating system divergence in secondary sympatry: testing an alternative hypothesis to reinforcement in Clarkia. Ann. Bot. 113:2223–35
    [Google Scholar]
  36. Brothers AN, Delph LF. 2017. Divergence in style length and pollen size leads to a postmating-prezygotic reproductive barrier among populations of Silene latifolia. Evolution 71:61532–40
    [Google Scholar]
  37. Brown BJ, Mitchell RJ. 2001. Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:143–49
    [Google Scholar]
  38. Bruckman D, Campbell DR. 2016. Timing of invasive pollen deposition influences pollen tube growth and seed set in a native plant. Biol. Invasions 18:61701–11
    [Google Scholar]
  39. Brys R, van Cauwenberghe J, Jacquemyn H 2016. The importance of autonomous selfing in preventing hybridization in three closely related plant species. J. Ecol. 104:2601–10
    [Google Scholar]
  40. Buerkle CA, Wolf DE, Rieseberg LH 2003. The origin and extinction of species through hybridization. Population Viability in Plants 165 CA Brigham, MW Schwartz 117–41 Berlin: Springer
    [Google Scholar]
  41. Burgess KS, Morgan M, Husband BC 2008. Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytol 177:1276–84
    [Google Scholar]
  42. Burke JM, Carney SE, Arnold ML 1998. Hybrid fitness in the Louisiana irises: analysis of parental and F1 performance. Evolution 52:37–43
    [Google Scholar]
  43. Campbell DR. 1985. Pollen and gene dispersal: the influences of competition for pollination. Evolution 39:2418–31
    [Google Scholar]
  44. Campbell DR, Motten AF. 1985. The mechanism of competition for pollination between two forest herbs. Ecology 66:2554–63
    [Google Scholar]
  45. Campbell DR, Waser NM. 2007. Evolutionary dynamics of an Ipomopsis hybrid zone: confronting models with lifetime fitness data. Am. Nat. 169:3298–310
    [Google Scholar]
  46. Campbell DR, Waser NM, Pederson GT 2002. Predicting patterns of mating and potential hybridization from pollinator behavior. Am Nat 159:5438–50
    [Google Scholar]
  47. Campbell DR, Waser NM, Wolf PG 1998. Pollen transfer by natural hybrids and parental species in an Ipomopsis hybrid zone. Evolution 52:61602–11
    [Google Scholar]
  48. Carney SE, Hodges SA, Arnold ML 1996. Effects of differential pollen-tube growth on hybridization in the Louisiana irises. Evol. Evol. 50:5051871–78
    [Google Scholar]
  49. Caruso CM, Alfaro M. 2000. Interspecific pollen transfer as a mechanism of competition: effect of Castilleja linariaefolia pollen on seed set of Ipomopsis aggregata. Can. J. Bot. 78:5600–6
    [Google Scholar]
  50. Castellanos MC, Wilson P, Thomson JD 2003. Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:122742
    [Google Scholar]
  51. Cheptou PO. 2019. Does the evolution of self-fertilization rescue populations or increase the risk of extinction. Ann. Bot. 123:1mcy144
    [Google Scholar]
  52. Chittka L, Thomson JD, Waser NM 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–77
    [Google Scholar]
  53. Christie K, Strauss SY. 2018. Along the speciation continuum: quantifying intrinsic and extrinsic isolating barriers across five million years of evolutionary divergence in California jewelflowers. Evolution 72:51063–79
    [Google Scholar]
  54. Clay DL, Novak SJ, Serpe MD, Tank DC, Smith JF 2012. Homoploid hybrid speciation in a rare endemic Castilleja from Idaho (Castilleja christii, Orobanchaceae). Am. J. Bot. 99:121976–90
    [Google Scholar]
  55. Coyne JA, Orr HA. 2004. Speciation Sunderland, MA: Sinauer
  56. De Jager ML, Dreyer LL, Ellis AG 2011. Do pollinators influence the assembly of flower colours within plant communities. Oecologia 166:543–53
    [Google Scholar]
  57. De Queiroz K. 2011. Branches in the lines of descent: Charles Darwin and the evolution of the species concept. Biol. J. Linn. Soc. 103:Jan.19–35
    [Google Scholar]
  58. Diaz A, Macnair MR. 1999. Pollen tube competition as a mechanism of prezygotic reproductive isolation between Mimulus nasutus and its presumed progenitor M. guttatus. New Phytol 144:3471–78
    [Google Scholar]
  59. Ducarme V, Vrancken J, Wesselingh RA 2010. Hybridization in annual plants: patterns and dynamics during a four-year study in mixed Rhinanthus populations. Folia Geobot 45:387–405
    [Google Scholar]
  60. Eaton DAR, Fenster CB, Hereford J, Huang S, Ree RH 2012. Floral diversity and community structure in Pedicularis (Orobanchaceae). Ecology 93:S182–93
    [Google Scholar]
  61. Ellstrand NC. 2014. Is gene flow the most important evolutionary force in plants. Am. J. Bot. 101:5737–53
    [Google Scholar]
  62. Emms SK, Arnold ML. 2000. Site-to-site differences in pollinator visitation patterns in a Louisiana iris hybrid zone. Oikos 91:568–78
    [Google Scholar]
  63. Fang Q, Huang S-Q. 2013. A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:51176–85
    [Google Scholar]
  64. Feinsinger P, Tiebout HM III 1991. Competition among plants sharing hummingbird pollinators: laboratory experiments on a mechanism. Ecology 72:61946–52
    [Google Scholar]
  65. Figueroa-Castro DM, Holtsford TP. 2009. Post-pollination mechanisms in Nicotiana longiflora and N. plumbaginifolia: pollen tube growth rate, offspring paternity and hybridization. Sex. Plant Reprod. 22:3187–96
    [Google Scholar]
  66. Fishman L, Aagaard J, Tuthill JC 2008. Toward the evolutionary genomics of gametophytic divergence: patterns of transmission ratio distortion in monkeyflower (Mimulus) hybrids reveal a complex genetic basis for conspecific pollen precedence. Evolution 62:122958–70
    [Google Scholar]
  67. Fishman L, Wyatt R. 1999. Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:61723–33
    [Google Scholar]
  68. Flanagan RJ, Mitchell RJ, Knutowski D, Karron JD 2009. Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). Am. J. Bot. 96:4809–15
    [Google Scholar]
  69. Galen C, Gregory T. 1989. Interspecific pollen transfer as a mechanism of competition: consequences of foreign pollen contamination for seed set in the alpine wildflower, Polemonium viscosum. Oecologia 81:120–23
    [Google Scholar]
  70. Gegear RJ, Laverty TM. 2005. Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim. Behav. 69:939–49
    [Google Scholar]
  71. Goodwillie C, Ness JM. 2013. Interactions of hybridization and mating systems: a case study in Leptosiphon (Polemoniaceae). Am. J. Bot. 100:61002–13
    [Google Scholar]
  72. Goulson D. 2000. Are insects flower constant because they use search images to find flowers. Oikos 88:547–52
    [Google Scholar]
  73. Grant V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. PNAS 91:13–10
    [Google Scholar]
  74. Grossenbacher D, Briscoe Runquist RD, Goldberg EE, Brandvain Y 2016. No association between plant mating system and geographic range overlap. Am. J. Bot. 103:1110–17
    [Google Scholar]
  75. Grossenbacher DL, Stanton ML. 2014. Pollinator-mediated competition influences selection for flower-color displacement in sympatric monkeyflowers. Am. J. Bot. 101:111915–24
    [Google Scholar]
  76. Grossenbacher DL, Whittall JB. 2011. Increased floral divergence in sympatric monkeyflowers. Evolution 65:92712–18
    [Google Scholar]
  77. Harder LD, Cruzan MB, Thomson JD 1993. Unilateral incompatibility and the effects of interspecific pollination for Erythronium americanum and Erythronium albidum (Liliaceae). Can. J. Bot. 71:2353–58
    [Google Scholar]
  78. Hasegawa Y, Suyama Y, Seiwa K 2015. Variation in pollen-donor composition among pollinators in an entomophilous tree species, Castanea crenata, revealed by single-pollen genotyping. PLOS ONE 10:31–15
    [Google Scholar]
  79. Heinrich B. 1975. Bee flowers: a hypothesis on flower variety and blooming times. Evolution 29:325–34
    [Google Scholar]
  80. Hipperson H, Dunning LT, Baker WJ, Butlin RK, Hutton I et al. 2016. Ecological speciation in sympatric palms: 2. Pre- and post-zygotic isolation. J. Evol. Biol. 29:112143–56
    [Google Scholar]
  81. Hopkins R. 2013. Reinforcement in plants. New Phytol 197:41095–1103
    [Google Scholar]
  82. Hopkins R, Rausher MD. 2012. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335:1090–92
    [Google Scholar]
  83. Howard DJ. 1999. Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Syst. 30:109–32
    [Google Scholar]
  84. Huang S-Q, Shi XQ. 2013. Floral isolation in Pedicularis: How do congeners with shared pollinators minimize reproductive interference. New Phytol 199:3858–65
    [Google Scholar]
  85. Huang Z-H, Liu H-L, Huang S-Q 2015. Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body. J. Plant Ecol. 8:2109–15
    [Google Scholar]
  86. Ippolito A, Fernandes GW, Holtsford TP 2004. Pollinator preferences for Nicotiana alata, N. forgetiana, and their F1 hybrids. Evolution 58:122634–44
    [Google Scholar]
  87. Jakobsson A, Padrón B, Traveset A 2008. Pollen transfer from invasive Carpobrotus spp. to natives—a study of pollinator behaviour and reproduction success. Biol. Conserv. 141:1136–45
    [Google Scholar]
  88. Johnson AL, Ashman T. 2019. Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phytol 221:142–54
    [Google Scholar]
  89. Johnson SD, Raguso RA. 2016. The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa. Ann. Bot. 117:125–36
    [Google Scholar]
  90. Kalisz S, Randle A, Chaiffetz D, Faigeles M, Butera A, Beight C 2012. Dichogamy correlates with outcrossing rate and defines the selfing syndrome in the mixed-mating genus Collinsia. Ann. Bot 109:3571–82
    [Google Scholar]
  91. Karrenberg S, Liu X, Hallander E, Favre A, Herforth-Rahmé J, Widmer A 2018. Ecological divergence plays an important role in strong but complex reproductive isolation in campions (Silene). Evolution 73:1–17
    [Google Scholar]
  92. Karron JD, Ivey CT, Mitchell RJ, Whitehead MR, Peakall R, Case AL 2012. New perspectives on the evolution of plant mating systems. Ann. Bot. 109:3493–503
    [Google Scholar]
  93. Kay KM. 2006. Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:3538–52
    [Google Scholar]
  94. Kay KM, Schemske DW. 2008. Natural selection reinforces speciation in a radiation of neotropical rainforest plants. Evolution 62:102628–42
    [Google Scholar]
  95. Kay KM, Zepeda AM, Raguso RA 2019. Experimental sympatry reveals geographic variation in floral isolation by hawkmoths. Ann. Bot. 123:405–13
    [Google Scholar]
  96. Kohn JR, Waser NM. 1985. The effect of Delphinium nelsonii pollen on seed set in Ipomopsis aggregata, a competitor for hummingbird pollination. Am. J. Bot. 72:1144–48
    [Google Scholar]
  97. Kostyun JL, Moyle LC. 2017. Multiple strong postmating and intrinsic postzygotic reproductive barriers isolate florally diverse species of Jaltomata (Solanaceae). Evolution 71:61556–71
    [Google Scholar]
  98. Laverty TM. 1994. Costs to foraging bumble bees of switching plant species. Can. J. Zool. 72:43–47
    [Google Scholar]
  99. Lloyd DG. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153:370–80
    [Google Scholar]
  100. Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH 2008. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. B 363:15063009–21
    [Google Scholar]
  101. Lyu N, Du W, Wang XF 2016. Unique growth paths of heterospecific pollen tubes result in late entry into ovules in the gynoecium of Sagittaria (Alismataceae). Plant Biol 19:2108–14
    [Google Scholar]
  102. Mallet J, Besansky N, Hahn MW 2016. How reticulated are species. BioEssays 38:2140–49
    [Google Scholar]
  103. Martin NH, Willis JH. 2007. Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:168–82
    [Google Scholar]
  104. Matallana G, Godinho MAS, Guilherme FAG, Belisario M, Coser TS, Wendt T 2010. Breeding systems of Bromeliaceae species: evolution of selfing in the context of sympatric occurrence. Plant Syst. Evol. 289:1–257–65
    [Google Scholar]
  105. McLernon SM, Murphy SD, Aarssen LW 1996. Heterospecific pollen transfer between sympatric species in a midsuccessional old-field community. Am. J. Bot. 83:1168–74
    [Google Scholar]
  106. Miller TJ, Raguso RA, Kay KM 2014. Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors. Ann. Bot. 113:2317–29
    [Google Scholar]
  107. Minder AM, Rothenbuehler C, Widmer A 2007. Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Mol. Ecol. 16:2504–16
    [Google Scholar]
  108. Minnaar C, Anderson B. 2019. Using quantum dots as pollen labels to track the fates of individual pollen grains. Methods Ecol. Evol. 10:5604–14
    [Google Scholar]
  109. Minnaar C, Anderson B, de Jager ML, Karron JD 2019. Plant–pollinator interactions along the pathway to paternity. Ann. Bot. 123:1225–45
    [Google Scholar]
  110. Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD 2009. New frontiers in competition for pollination. Ann. Bot. 103:91403–13
    [Google Scholar]
  111. Montgomery BR, Soper DM, Delph LF 2010. Asymmetrical conspecific seed-siring advantage between Silene latifolia and S. dioica. Ann. Bot. 105:4595–605
    [Google Scholar]
  112. Morales CL, Traveset A. 2008. Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit. Rev. Plant Sci. 27:4221–38
    [Google Scholar]
  113. More M, Sersic AN, Cocucci AA 2007. Restriction of pollinator assemblage through flower length and width in three long-tongued hawkmoth-pollinated species of Mandevilla (Apocynaceae, Apocynoideae). Ann. Mo. Bot. Gard. 94:2485–504
    [Google Scholar]
  114. Muchhala N. 2006. The pollination biology of Burmeistera (Campanulaceae): specialization and syndromes. Am. J. Bot. 93:1081–89
    [Google Scholar]
  115. Muchhala N. 2007. Adaptive trade-off in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds. Am. Nat. 169:4494–504
    [Google Scholar]
  116. Muchhala N. 2008. Functional significance of interspecific variation in Burmeistera flower morphology: evidence from nectar bat captures in Ecuador. Biotropica 40:3332–37
    [Google Scholar]
  117. Muchhala N, Brown Z, Armbruster WS, Potts MD 2010. Competition drives specialization in pollination systems through costs to male fitness. Am. Nat. 176:6732–43
    [Google Scholar]
  118. Muchhala N, Caiza A, Vizuete JC, Thomson JD 2009. A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus. Ann. Bot. 103:91481–87
    [Google Scholar]
  119. Muchhala N, Jarrín-V P. 2002. Flower visitation by bats in cloud forests of Western Ecuador. Biotropica 34:3387–95
    [Google Scholar]
  120. Muchhala N, Johnsen S, Smith SD 2014. Competition for hummingbird pollination shapes flower color variation in Andean Solanaceae. Evolution 68:82275–86
    [Google Scholar]
  121. Muchhala N, Potts MD. 2007. Character displacement among bat-pollinated flowers of the genus Burmeistera: analysis of mechanism, process and pattern. Proc. Biol. Sci. 274:2731–37
    [Google Scholar]
  122. Muchhala N, Thomson JD. 2012. Interspecific competition in pollination systems: costs to male fitness via pollen misplacement. Funct. Ecol. 26:2476–82
    [Google Scholar]
  123. Muir G, Dixon CJ, Harper AL, Filatov DA 2012. Dynamics of drift, gene flow, and selection during speciation in Silene. Evolution 66:1447–58
    [Google Scholar]
  124. Murcia C, Feinsinger P. 1996. Interspecific pollen loss by hummingbirds visiting flower mixtures: effects of floral architecture. Ecology 77:2550–60
    [Google Scholar]
  125. Murphy SD, Aarssen LW. 1995. Allelopathic pollen extract from Phleum pratense L. (Poaceae) reduces germination, in vitro, of pollen of sympatric species. Int. J. Plant Sci. 156:425–34
    [Google Scholar]
  126. Natalis LC, Wesselingh RA. 2012a. Shared pollinators and pollen transfer dynamics in two hybridizing species, Rhinanthus minor and R. angustifolius. Oecologia 170:3709–21
    [Google Scholar]
  127. Natalis LC, Wesselingh RA. 2012b. Post-pollination barriers and their role in asymmetric hybridization in Rhinanthus (Orobanchaceae). Am. J. Bot. 99:111847–56
    [Google Scholar]
  128. Natalis LC, Wesselingh RA. 2013. Parental frequencies and spatial configuration shape bumblebee behavior and floral isolation in hybridizing Rhinanthus. Evolution 67:1692–705
    [Google Scholar]
  129. Ne'eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A 2010. A framework for comparing pollinator performance: effectiveness and efficiency. Biol. Rev. 85:3435–51
    [Google Scholar]
  130. Newman E, Manning J, Anderson B 2015. Local adaptation: mechanical fit between floral ecotypes of Nerine humilis (Amaryllidaceae) and pollinator communities. Evolution 69:92262–75
    [Google Scholar]
  131. Ollerton J, Winfree R, Tarrant S 2011. How many flowering plants are pollinated by animals. Oikos 120:3321–26
    [Google Scholar]
  132. Ortiz-Barrientos D, Grealy A, Nosil P 2009. The genetics and ecology of reinforcement: implications for the evolution of prezygotic isolation in sympatry and beyond. Ann. N.Y. Acad. Sci. 1168:156–82
    [Google Scholar]
  133. Ostevik KL, Andrew RL, Otto SP, Rieseberg LH 2016. Multiple reproductive barriers separate recently diverged sunflower ecotypes. Evolution 70:2322–35
    [Google Scholar]
  134. Oyama RK, Jones KN, Baum DA 2010. Sympatric sister species of Californian Antirrhinum and their transiently specialized pollinators. Am. Midl. Nat. 164:337–47
    [Google Scholar]
  135. Palmer M, Travis J, Antonovics J 1989. Temporal mechanisms influencing gender expression and pollen flow within a self-incompatible perennial, Amianthium muscaetoxicum (Liliaceae). Oecologia 78:231–36
    [Google Scholar]
  136. Paudel BR, Burd M, Shrestha M, Dyer AG, Li QJ 2018. Reproductive isolation in alpine gingers: how do coexisting Roscoea (R. purpurea and R. tumjensis) conserve species integrity. Evolution 72:91840–50
    [Google Scholar]
  137. Payseur BA, Rieseberg LH. 2016. A genomic perspective on hybridization and speciation. Mol. Ecol. 25:112337–60
    [Google Scholar]
  138. Pettengill JB, Moeller DA. 2012. Tempo and mode of mating system evolution between incipient Clarkia species. Evolution 66:1210–25
    [Google Scholar]
  139. Ramsey J, Bradshaw HD, Schemske DW 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:71520–34
    [Google Scholar]
  140. Randall JL, Hilu KW. 1990. Interference through improper pollen transfer in mixed stands of Impatiens capensis and I. pallida (Balsaminaceae). Am. J. Bot. 77:939–44
    [Google Scholar]
  141. Randle AM, Spigler RB, Kalisz S 2018. Shifts to earlier selfing in sympatry may reduce costs of pollinator sharing. Evolution 72:81587–99
    [Google Scholar]
  142. Rathcke BJ. 1983. Competition and facilitation among plants for pollination. Pollination Biology L Real 305–29 New York: Academic
    [Google Scholar]
  143. Rausher MD. 2017. Selfing, local mate competition, and reinforcement. Am. Nat. 189:287–104
    [Google Scholar]
  144. Renaut S, Rowe HC, Ungerer MC, Rieseberg LH 2014. Genomics of homoploid hybrid speciation: diversity and transcriptional activity of long terminal repeat retrotransposons in hybrid sunflowers. Philos. Trans. R. Soc. B 369:164820130345
    [Google Scholar]
  145. Roda F, Mendes FK, Hahn MW, Hopkins R 2017. Genomic evidence of gene flow during reinforcement in Texas Phlox. Mol. Ecol. 26:2317–30
    [Google Scholar]
  146. Rodríguez-Gironés MA, Santamaría L. 2007. Resource competition, character displacement, and the evolution of deep corolla tubes. Am. Nat. 170:455–64
    [Google Scholar]
  147. Ruane LG, Donohue K. 2008. Pollen competition and environmental effects on hybridization dynamics between Phlox drummondii and Phlox cuspidata. Evol. Ecol. 22:229–41
    [Google Scholar]
  148. Schiestl FP, Schlüter PM. 2009. Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu. Rev. Entomol. 54:425–46
    [Google Scholar]
  149. Schmickl R, Marburger S, Bray S, Yant L, Henderson I 2017. Hybrids and horizontal transfer: introgression allows adaptive allele discovery. J. Exp. Bot. 68:205453–70
    [Google Scholar]
  150. Schouppe D, Brys R, Vallejo-Marín M, Jacquemyn H 2017. Geographic variation in floral traits and the capacity of autonomous selfing across allopatric and sympatric populations of two closely related Centaurium species. Sci. Rep. 7:April46410
    [Google Scholar]
  151. Scribailo R, Barrett S. 1994. Effects of prior self-pollination on outcrossed seed set in tristylous Pontederia sagittata (Pontederiaceae). Sex. Plant Reprod. 7:273–81
    [Google Scholar]
  152. Shore JS, Barrett SC. 1984. The effect of pollination intensity and incompatible pollen on seed set in Turnera ulmifolia (Turneraceae). Can. J. Bot. 62:1298–303
    [Google Scholar]
  153. Sicard A, Lenhard M. 2011. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann. Bot. 107:91433–43
    [Google Scholar]
  154. Smith RA, Rausher MD. 2008. Experimental evidence that selection favors character displacement in the ivyleaf morning glory. Am. Nat. 171:11–9
    [Google Scholar]
  155. Sobel JM, Chen GF. 2014. Unification of methods for estimating the strength of reproductive isolation. Evolution 68:1511–22
    [Google Scholar]
  156. Sobel JM, Streisfeld MA. 2014. Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus. Evolution 69:447–61
    [Google Scholar]
  157. Stankowski S, Streisfeld MA. 2015. Introgressive hybridization facilitates adaptive divergence in a recent radiation of monkeyflowers. Proc. R. Soc. B 282:181420151666
    [Google Scholar]
  158. Surget-Groba Y, Kay KM. 2013. Restricted gene flow within and between rapidly diverging Neotropical plant species. Mol. Ecol. 22:194931–42
    [Google Scholar]
  159. Takahashi Y, Takakura KI, Kawata M 2016. Spatial distribution of flower color induced by interspecific sexual interaction. PLOS ONE 11:10e0164381
    [Google Scholar]
  160. Temeles EJ, Mazzotta AR, Williamson A 2017. Resource partitioning by color in a tropical hummingbird. Behav. Ecol. Sociobiol. 71:129
    [Google Scholar]
  161. Thomson JD, Andrews BJ, Plowright RC 1982. The effect of foreign pollen on ovule development in Diervilla lonicera (Caprifoliaceae). New Phytol 90:777–83
    [Google Scholar]
  162. Thomson JD, Fung HF, Ogilvie JE 2018. Effects of spatial patterning of co-flowering plant species on pollination quantity and purity. Ann. Bot. 123:2303–10
    [Google Scholar]
  163. Tiffin P, Olson MS, Moyle LC 2001. Asymmetrical crossing barriers in angiosperms. Proc. R. Soc. B 268:1469861–67
    [Google Scholar]
  164. Tscheulin T, Petanidou T, Potts SG, Settele J 2009. The impact of Solanum elaeagnifolium, an invasive plant in the Mediterranean, on the flower visitation and seed set of the native co-flowering species Glaucium flavum. Plant Ecol 205:177–85
    [Google Scholar]
  165. Tur C, Sáez A, Traveset A, Aizen MA 2016. Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: evidence of widespread facilitation in south Andean plant communities. Ecol. Lett. 19:5576–86
    [Google Scholar]
  166. Vallejo-Marín M, Cooley AM, Lee MY, Folmer M, McKain MR, Puzey JR 2016. Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor. Am. J. Bot. 103:71272–88
    [Google Scholar]
  167. Vallejo-Marín M, Hiscock SJ. 2016. Hybridization and hybrid speciation under global change. New Phytol 211:1170–87
    [Google Scholar]
  168. Vallejo-Marín M, Walker C, Friston-Reilly P, Solís-Montero L, Igic B 2014. Recurrent modification of floral morphology in heterantherous Solanum reveals a parallel shift in reproductive strategy. Philos. Trans. R. Soc. B 369:164920130256
    [Google Scholar]
  169. Vrancken J, Brochmann C, Wesselingh RA 2012. A European phylogeography of Rhinanthus minor compared to Rhinanthus angustifolius: unexpected splits and signs of hybridization. Ecol. Evol. 2:1531–48
    [Google Scholar]
  170. Wang J, Cruzan MB. 1998. Interspecific mating in the Piriqueta caroliniana (Turneraceae) complex: effects of pollen load size and composition. Am. J. Bot. 85:91172–79
    [Google Scholar]
  171. Waser NM. 1978a. Interspecific pollen transfer and competition between co-occurring plant species. Oecologia 36:2223–36
    [Google Scholar]
  172. Waser NM. 1978b. Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59:5934–44
    [Google Scholar]
  173. Waser NM. 1983. Competition for pollination and floral character differences among sympatric plant species: a review of the evidence. Handbook of Experimental Pollination Biology CE Jones, RJ Little 277–93 New York: Van Nostrand Reinhold
    [Google Scholar]
  174. Waser NM. 1986. Flower constancy: definition, cause, and measurement. Am. Nat. 127:593–603
    [Google Scholar]
  175. Waser NM, Fugate ML. 1986. Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphiniium nelsonii and Ipomopss aggregata. Oecologia 70:573–77
    [Google Scholar]
  176. Weber MG, Cacho NI, Phan MJQ, Disbrow C, Ramírez SR, Strauss SY 2018. The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.). Evolution 72:4798–807
    [Google Scholar]
  177. Whitehead MR, Lanfear R, Mitchell RJ, Karron JD 2018. Plant mating systems often vary widely among populations. Front. Ecol. Evol. 6:April1–9
    [Google Scholar]
  178. Whitney KD, Randell RA, Rieseberg LH 2010. Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 187:1230–39
    [Google Scholar]
  179. Whitton J, Sears CJ, Maddison WP 2017. Co-occurrence of related asexual, but not sexual, lineages suggests that reproductive interference limits coexistence. Proc. R. Soc. B 284:186820171579
    [Google Scholar]
  180. Wilson P, Stine M. 1996. Floral constancy in bumble bees: handling efficiency or perceptual conditioning. Oecologia 106:493–99
    [Google Scholar]
  181. Wolf PG, Campbell DR, Waser NM, Sipes SD, Toler TR, Archibald JK 2001. Tests of pre- and postpollination barriers to hybridization between sympatric species of Ipomopsis (Polemoniaceae). Am. J. Bot. 88:2213–19
    [Google Scholar]
  182. Wu CA, Campbell DR. 2005. Cytoplasmic and nuclear markers reveal contrasting patterns of spatial genetic structure in a natural Ipomopsis hybrid zone. Mol. Ecol. 14:781–92
    [Google Scholar]
  183. 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. Linn. Soc. 90:137–48
    [Google Scholar]
  184. Zhang J-J, Montgomery BR, Huang S-Q 2016. Evidence for asymmetrical hybridization despite pre- and post-pollination reproductive barriers between two Silene species. AoB PLANTS 8:plw032
    [Google Scholar]
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