Evolutionary Ecology

, Volume 29, Issue 3, pp 355–377 | Cite as

Convergence of anti-bee pollination mechanisms in the Neotropical plant genus Drymonia (Gesneriaceae)

  • John L. ClarkEmail author
  • Laura Clavijo
  • Nathan Muchhala
Original Paper


The neotropical plant genus Drymonia displays a remarkable variety of floral shapes and colors. One feature that is particularly important to coevolution with pollinators involves the variable shapes and widths of corolla tubes. To evaluate the evolutionary context for changes in corolla shape, we constructed a phylogeny of 50 of the 75 species of Drymonia using molecular markers from plastid (trnK-matK) and nuclear regions (ITS and ETS). Mapping tube shapes on the phylogeny supports open, bell-shaped (campanulate) corolla shape as the ancestral character state for Drymonia, with multiple independent origins of constriction in the corolla tube. Corollas with constrictions take one of three tube shapes: a constricted flower opening and throat with a large, expanded pouch on the lower surface (hypocyrtoid); a constricted flower opening and throat lacking an expanded pouch on the lower surface (urceolate); or a constricted opening and throat where the sides of the corolla appear laterally compressed. Fieldwork demonstrates euglossine bees (mostly Euglossa spp. and Epicharis spp.) visit campanulate corollas while hummingbirds visit corollas that are constricted. Results support eight independent origins of constricted corolla tubes from ancestors with campanulate corolla tubes: 3 hypocyrtoid clades, 3 laterally compressed clades, and 3 urceolate clades (one of which represents a shift from a hypocyrtoid ancestor). Constricted corollas are associated with shifts from the ancestral condition of poricidal anther dehiscence, which presents pollen to pollinators in multiple small doses, to the derived condition of longitudinal anther dehiscence, which presents all pollen to pollinators simultaneously. The association of hummingbird pollination with constricted corolla tubes suggests that narrowing evolved as a barrier mechanism that prohibits the visitation of flowers by bees.


Convergence Drymonia Gesneriaceae Hypocyrtoid corollas Laterally compressed corollas Pollination biology Poricidal anther dehiscence Urceolate corollas 



The authors would like to thank Alex Monro from The Natural History Museum in London (BM) for sharing leaf material of Gesneriaceae. This study was supported by grants from the National Science Foundation (DEB-0949270 and DEB-0841958 to JLC). Fieldwork was greatly facilitated by the following undergraduate students from The University of Alabama: Cassandra L. Coleman, Seema Kumar, and Laura A. Frost. Lucas McDonald from Hillcrest High School (Tuscaloosa, AL) also helped in collecting data during a 2011 expedition to Ecuador. Murray Cooper and Richard W. Dunn are gratefully acknowledged for contributing images. We express our appreciation to two anonymous reviewers for useful comments that improved an earlier version of the manuscript.


  1. Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Mol Phylogenet Evol 10:449–463CrossRefPubMedGoogle Scholar
  2. Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277CrossRefGoogle Scholar
  3. Barker FK, Lutzoni FM (2002) The utility of the incongruence length difference test. Syst Biol 51:625–637CrossRefPubMedGoogle Scholar
  4. Beardsley PM, Olmstead RG (2002) Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma. Am J Bot 89:1093–1102CrossRefPubMedGoogle Scholar
  5. Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 73–113Google Scholar
  6. Burtt BL, Wiehler H (1995) Classification of the family Gesneriaceae. Gesneriana 1:1–4Google Scholar
  7. Buzato S, Sazima M, Sazima I (2000) Hummingbird-pollinated floras at three Atlantic forest sites. Biotropica 32:824–841CrossRefGoogle Scholar
  8. Castellanos MC, Wilson P, Keller SJ, Wolfe AD, Thomson JD (2006) Anther evolution: pollen presentation strategies when pollinators differ. Am Nat 167:288–296CrossRefPubMedGoogle Scholar
  9. Clark JL (2005) A Monograph of Alloplectus (Gesneriaceae). Selbyana 25:182–209Google Scholar
  10. Clark JL (2009) The systematics of Glossoloma (Gesneriaceae). Syst Bot Monogr 88:1–128Google Scholar
  11. Clark JL, Herendeen PS, Skog LE, Zimmer EA (2006) Phylogenetic relationships and generic boundaries in the tribe Episcieae (Gesneriaceae) inferred from nuclear, chloroplast, and morphological data. Taxon 55:313–336CrossRefGoogle Scholar
  12. Clark JL, Funke MM, Duffy AM, Smith JF (2012) Phylogeny of a Neotropical clade in the Gesneriaceae: more tales of convergent evolution. Int J Plant Sci 173:894–916CrossRefGoogle Scholar
  13. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedGoogle Scholar
  14. Dolphin K, Belshaw R, Orme CDL, Donald L, Quicke J (2000) Noise and incongruence: interpreting results of the incongruence length difference test. Mol Phylogenet Evol 17:401–406CrossRefPubMedGoogle Scholar
  15. Dowton M, Austin AD (2002) Increased congruence does not necessarily indicate increased phylogenetic accuracy: the behavior of the incongruence length difference test in mixed-model analyses. Syst Biol 51:19–31CrossRefPubMedGoogle Scholar
  16. Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210CrossRefGoogle Scholar
  17. Dziedzioch C, Stevens AD, Gottsberger G (2003) The hummingbird plant community of a tropical montane rain forest in southern Ecuador. Plant Biol 5:331–337CrossRefGoogle Scholar
  18. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedCentralPubMedGoogle Scholar
  19. Enrique ERA (1998) Resources foraged by Euglossa atroveneta (Apidae: Euglossinae) at Union Juárez, Chiapas, Mexico. A palynological study of larval feeding. Apidologie 29:347–359CrossRefGoogle Scholar
  20. Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon, OxfordGoogle Scholar
  21. Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  22. Feinsinger P, Beach JH, Linhart YB, Rusby WH, Murray KG (1987) Disturbance, pollinator predictability, and pollination success among Costa Rican cloud forest plants. Ecology 68:1294–1305CrossRefGoogle Scholar
  23. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  24. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol S 35:375–403CrossRefGoogle Scholar
  25. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–415CrossRefGoogle Scholar
  26. Franco ALM, Buzato S (1992) An assemblage of hummingbird-pollinated flowers in a montane forest in southeastern Brazil. Bot Acta 109:149–160Google Scholar
  27. Fritsch K (1893–1994) Gesneriaceae. In: Engler A, Prantl K (eds) Die Nat. Pflanzenfam., vol 4 (3b). Engelmann, Leipzig, Germany, pp 133–185Google Scholar
  28. Goloboff P (1999) NONA, version 2. Published by the author, TucumánGoogle Scholar
  29. Grant KA, Grant V (1968) Hummingbirds and their flowers. Columbia University Press, New YorkGoogle Scholar
  30. Grant V, Temeles EJ (1992) Foraging ability of rufous hummingbirds on hummingbird flowers and hawkmoth flowers. Proc Natl Acad Sci 89(20):9400–9404CrossRefPubMedCentralPubMedGoogle Scholar
  31. Hanstein J (1854) Die Gesneraceen des Königlichen Herbariums und der Gärten zu Berlin, nebst Beobachtungen über die Familie im Ganzen I. Abschnitt. Linnaea 26:145–216Google Scholar
  32. Hanstein J (1856) Die Gesneraceen des Königlichen Herbariums und der Gärten zu Berlin, nebst monographischer Uebersicht der Familie im Ganzen, II. Abschnitt. Gattungen und Arten. Erstes Stück. Die Niphaeen und Achimeneen. Linnaea 27:693–785Google Scholar
  33. Hanstein J (1859) Die Gesneraceen des Königlichen Herbariums und der Garten zu Berlin, nebst monographischer Uebersicht der Familie im Ganzen, II. Abschnitt. Gattungen und Arten. Zweites Stück. Die Brachylomateen. Linnaea 29:497–592Google Scholar
  34. Hanstein J (1865) Die Gesneraceen des Königlichen Herbariums und der Gärten zu Berlin, nebst monographischer Uebersicht der Familie im Ganzen, II. Abschnitt. Gattungen und Arten. Drittes Stück. Die Eugesnereen, Rhytidophylleen, und Beslerieen. Linnaea 34:225–462Google Scholar
  35. Harder LD (1990) Pollen removal by bumble bees and its implications for pollen dispersal. Ecology 71:1110–1125CrossRefGoogle Scholar
  36. Harder L, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am Nat 133:325–334CrossRefGoogle Scholar
  37. Ivanina LI (1965) Application of the carpological method to the taxonomy of Gesneriaceae. Notes Roy Bot Gard Edinburgh 26:383–402Google Scholar
  38. Ivanina LI (1967) The family Gesneriaceae (The Carpological Review). Komarov Bot. Inst, Leningrad, USSR, 126 ppGoogle Scholar
  39. Johnson LA, Soltis DE (1995) Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Ann Missouri Bot Gard 82:149–175CrossRefGoogle Scholar
  40. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. Accessed March 2014
  41. Martius CFP (1829) Gesneriaceae. Nova Genera et Species Plantarum, vol 3. Impensis auctoris, Munich, pp 27–73Google Scholar
  42. Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545CrossRefGoogle Scholar
  43. Miller MA, Holder MT, Vos R, Midford PE, Liebowitz T, Chan L, Hoover P, Warnow T (2009) The CIPRES Portals. CIPRES. 2009–08–04. Accessed March 2014
  44. Möller M, Clark JL (2013) The state of molecular studies in the family Gesneriaceae. Selbyana 31:95–125Google Scholar
  45. Moore HE (1955) Drymonia macrophylla. Baileya 3:109–112Google Scholar
  46. Muchhala N (2007) Adaptive tradeoff in floral morphology mediates specialization for flowers pollinated by bats and hummingbirds. Am Nat 169:494–504CrossRefPubMedGoogle Scholar
  47. Nixon KC (1999) The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414CrossRefGoogle Scholar
  48. Nixon KC (2002) WinClada, version 1.00.08. Published by the author, Ithaca, New YorkGoogle Scholar
  49. Rambaut A, Drummond AJ (2007) Tracer v1.4: MCMC trace analyses tool. Accessed October 25, 2013
  50. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedCentralPubMedGoogle Scholar
  51. San Martin-Gajardo I, Santana Vianna JR (2010) Pollination of Namatanthus brasiliensis: an epiphytic Gesneriaceae endemic to the southeastern Atlantic forests of Brazil. Selbyana 30:216–220Google Scholar
  52. Sazima I, Buzato S, Sazima M (1995) An assemblage of hummingbird-pollinated flowers in a montane forest in southeastern Brazil. Bot Acta 109:149–160CrossRefGoogle Scholar
  53. Seelanen T, Schnabel A, Wendel JF (1997) Congruence and consensus in the cotton tribe (Malvaceae). Syst Bot 22:259–290CrossRefGoogle Scholar
  54. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  55. Smith JF, Atkinson S (1998) Phylogenetic analysis of the tribes Gloxinieae and Gesnerieae (Gesneriaceae): data from ndhF sequences. Selbyana 19:122–131Google Scholar
  56. Smith JF, Clark JL (2013) Molecular phylogenetic analyses reveal undiscovered monospecific Genera in the tribe Episcieae (Gesneriaceae). Syst Bot 38:451–463CrossRefGoogle Scholar
  57. Smith JF, Wolfram JC, Brown KD, Carroll CL, Denton DS (1997) Tribal relationships in the Gesneriaceae: evidence from DNA sequences of the chloroplast gene ndhF. Ann Missouri Bot Gard 84:50–66CrossRefGoogle Scholar
  58. Smith JF, Kresge M, Møller M, Cronk QCB (1998) The African violets (Saintpaulia) are members of Streptocarpus subgenus Streptocarpella (Gesneriaceae): combined evidence from chloroplast and nuclear ribosomal genes. Edinb J Bot 55:1–11CrossRefGoogle Scholar
  59. Smith JF, Draper SB, Hileman LC, Baum DA (2004a) A phylogenetic analysis within tribes Gloxinieae and Gesnerieae (Gesnerioideae: Gesneriaceae). Syst Bot 29:947–958CrossRefGoogle Scholar
  60. Smith JF, Draper SB, Hileman LC, Baum DA (2004b) Evolution of GCYC, a Gesneriaceae homolog of CYCLOIDEA, within Gesnerioideae (Gesneriaceae). Mol Phylog Evol 31:765–779CrossRefGoogle Scholar
  61. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  62. Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 5:758–771CrossRefGoogle Scholar
  63. Steiner KE (1985) The role of nectar and oil in the pollination of Drymonia serrulata (Gesneriaceae) by Epicharis bees (Anthophorideae) in Panama. Biotropica 17:217–229CrossRefGoogle Scholar
  64. Stiles FG, Freeman CE (1993) Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25:191–205CrossRefGoogle Scholar
  65. Suh Y, Thien LB, Reeve HE, Zimmer EA (1993) Molecular evolution and phylogenetic implications of internal transcribed spacer sequences of ribosomal DNA in Winteraceae. Am J Bot 80:1042–1055CrossRefGoogle Scholar
  66. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods), Version 4.0. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  67. Temeles EJ, Linhart RB, Masonjones M, Masonjones HD (2002) The role of flower width in hummingbird bill length-flower length relationships. Biotropica 34:68–80Google Scholar
  68. Thiers B (2013) [continuously updated]: Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden. Accessed March 2013
  69. Thomson JD, Thomson BA (1992) Pollen presentation and viability schedules in animal-pollinated plants: consequences for reproductive success. In: Wyatt R (ed) Ecology and evolution of plant reproduction: new approaches. Chapman and Hall, New York, pp 1–24Google Scholar
  70. Thomson JD, Wilson P, Valenzuela M, Malzone M (2000) Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biol 15:11–29CrossRefGoogle Scholar
  71. Weber A, Clark JL, Möller M (2013) A new formal classification of Gesneriaceae. Selbyana 31:68–94Google Scholar
  72. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322CrossRefGoogle Scholar
  73. Wiehler H (1973) 100 Transfers from Alloplectus and Columnea (Gesneriaceae). Phytologia 27:309–329Google Scholar
  74. Wiehler H (1983) A synopsis of the Neotropical Gesneriaceae. Selbyana 6:1–219Google Scholar
  75. Willson MF, Thompson JN (1982) Phenology and ecology of color in bird-dispersed fruits, or why some fruits are red when they are “green”? Can J Bot 60:701–713CrossRefGoogle Scholar
  76. Wolf LL, Stiles FJ (1989) Adaptations for the ‘Fail-safe’ pollination of specialized ornithophilous flowers. Am Midl Nat 121:1–10CrossRefGoogle Scholar
  77. Yoder AD, Irwin JA, Payseur BA (2001) Failure of the ILD to determine data combinability for slow loris phylogeny. Syst Biol 50:408–424CrossRefPubMedGoogle Scholar
  78. Zimmer EA, Roalson EH, Skog LE, Boggan JK, Idnurm A (2002) Phylogenetic relationships in the Gesnerioideae (Gesneriaceae) based on nrDNA ITS and cpDNA trnL-F and trnE-T spacer region sequences. Am J Bot 89:296–311CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • John L. Clark
    • 1
    Email author
  • Laura Clavijo
    • 1
  • Nathan Muchhala
    • 2
  1. 1.Department of Biological SciencesThe University of AlabamaTuscaloosaUSA
  2. 2.Department of BiologyUniversity of Missouri-St. LouisSt. LouisUSA

Personalised recommendations