Sexual isolation in two bee-pollinated Costus (Costaceae)

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Examining reproductive isolating barriers is essential for understanding processes of speciation. Sexual isolation has been shown to contribute to speciation in many sympatric taxa; however, its role in parapatric taxa with reduced interspecific gene flow is poorly understood. I investigated the extent of sexual isolation in two closely related Neotropical understory species, Costus allenii and C. villosissimus, that occur in adjacent habitats within flight distance of their shared pollinators, euglossine bees. Pollination arrays were used to test whether individual pollinators travel between species, to estimate the proportion of hetero- and conspecific pollen deposited on the stigmas, and to examine the proportion of hybrid progeny. In comparison to C. allenii, C. villosissimus produces flowers with larger labella, longer stamen–labellum distances, and longer styles. Pollinators visited both species but preferred C. villosissimus. This preference caused pollinator isolation in C. villosissimus. In C. allenii, the frequency of heterospecific pollinator transitions was not less common than that of conspecific transitions, but floral mechanical isolation greatly reduced the likelihood of heterospecific pollen deposition. The contribution of gametic isolation was not strong in either species. Based on data for pollinator isolation, floral mechanical isolation, and gametic isolation, it appears that sexual isolation is weak in C. allenii, restricting heterospecific gene flow by 25 %, but moderate in C. villosissimus, where gene flow from C. allenii is reduced by 70 %. Further research will estimate the magnitude of other isolation barriers to determine the relative contribution of sexual isolation to total isolation in this parapatric species pair.

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  1. Albert AYK, Schluter D (2004) Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection? Evolution 58:1099–1107

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

  3. Andalo C, Cruzan MB, Cazattes C, Pujol B, Burrus M, Thébaud C (2010) Post-pollination barriers do not explain the persistence of two distinct Antirrhinum subspecies with parapatric distribution. Plant Syst Evol 286:223–234

  4. Boose DL (1997) Sources of variation in floral nectar production rate in Epilobium canum (Onagraceae): implications for natural selection. Oecologia 110:493–500

  5. Campbell DR (2008) Pollinator shifts and the origin and loss of plant species. Ann Missouri Bot Gard 95:264–274

  6. Campbell DR, Waser NM (2007) Evolutionary dynamics of an Ipomopsis hybrid zone: confronting models with lifetime fitness data. Am Nat 169:298–310

  7. Campbell DR, Bischoff M, Lord JM, Robertson AW (2010) Flower color influences insect visitation in alpine New Zealand. Ecology 91:2638–2649

  8. Carroll AB, Pallardy ST, Galen C (2001) Drought stress, plant water status, and floral trait expression in fireweed, Epilobium angustifolium (Onagraceae). Am J Bot 88:438–446

  9. Chari J, Wilson P (2001) Factors limiting hybridization between Penstemon spectabilis and Penstemon centranthifolius. Can J Bot 79:1439–1448

  10. Chen GF (2011) Experimental studies of adaptation and speciation in two Neotropical Costus species. Dissertation, Michigan State University

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

  12. Coyne JA, Orr HA (1997) “Patterns of speciation in Drosophila” revisited. Evolution 51:295–303

  13. Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

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

  15. Dopman EB, Robbins PS, Seaman A (2010) Components of reproductive isolation between North America pheromone strains of the European corn borer. Evolution 64:881–902

  16. Dressler RL (1982) Biology of the orchid bees (Euglossini). Ann Rev Ecol Syst 13:373–394

  17. Escobar-Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science 317:656–660

  18. 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(4):809–815

  19. Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc R Soc Lond B 266:2247–2252

  20. Gavrilets S, Cruzan MB (1998) Neutral gene flow across single locus clines. Evolution 52:1277–1284

  21. Gegear RJ, Laverty TM (2005) Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim Behav 69:939–949

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

  23. Halpern SL, Adler LS, Wink M (2010) Leaf herbivory and drought stress affect floral attractive and defensive traits in Nicotiana quadrivalvis. Oecologia 163:961–971

  24. Harder LD (1982) Measurement and estimation of functional proboscis length in bumblebees (Hymenoptera: Apidae). Can J Zool 60:1073–1079

  25. Harder LD (1983) Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57:274–280

  26. Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545

  27. Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866–873

  28. Heslop-Harrison J (1982) Pollen–stigma interaction and cross-incompatibility in the grasses. Science 215:1358–1364

  29. Hill KL, L’Hernault SW (2001) Analyses of reproductive interactions that occur after heterospecific mating within the genus Caenorhabditis. Dev Biol 232:105–114

  30. Hurt CR, Farzin M, Hedrick PW (2005) Examining the process of allopatric speciation in the endangered Sonoran topminnow using cytonuclear genotype frequencies. Genetics 71:655–672

  31. Husband BC, Sabara HA (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol 161:703–713

  32. Husband BC, Schemske DW (2000) Ecological mechanisms of reproductive isolation between diploid and tetraploid Chamerion angustifolium. J Ecol 88:689–701

  33. Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205

  34. Jones KN (1997) Analysis of pollinator foraging: tests for non-random behavior. Funct Ecol 11:255–259

  35. Kay KM (2006) Reproductive isolation between two closely related hummingbird-pollinated Neotropical gingers. Evolution 60:538–552

  36. Kay KM, Schemske DW (2008) Natural selection reinforces speciation in a radiation of Neotropical rainforest plants. Evolution 62:2628–2642

  37. Kay KM, Reeves PA, Olmstead RG, Schemske DW (2005) Rapid speciation and evolution of hummingbird pollination in Neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA ITS and ETS sequences. Am J Bot 92:1899–1910

  38. Kimsey LS (1984) The behavioural and structural aspects of grooming and related activities in euglossine bees (Hymenoptera: Apidae). J Zool 204:541–550

  39. Klips RA (1999) Pollen competition as a reproductive isolating mechanisms between two sympatric Hisbiscus species (Malvaceae). Am J Bot 86:269–272

  40. Levin DA (1978) The origin of isolating mechanisms in flowering plants. Evol Biol 11:185–317

  41. Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos T R Soc B 363:3009–3021

  42. Maas PJM (1972) Costoideae (Zingiberaceae). Flora Neotropica, monograph 8. Hafner, New York

  43. Mallet J (2006) What does Drosophila genetics tell us about speciation? Trends Ecol Evol 21(7):386–393

  44. Martin NH, Willis JH (2007) Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68–82

  45. Matsubayashi KW, Katakura H (2009) Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution 63:2563–2580

  46. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

  47. Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288

  48. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

  49. Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD (2009) Ecology and evolution of plant–pollinator interactions. Ann Bot-Lond 103:1355–1363

  50. Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant–pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40

  51. Nosil P (2007) Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am Nat 169:151–162

  52. Nosil P, Vines TH, Funk DJ (2005) Prospective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

  53. Palumbi SR, Metz EC (1991) Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol 8:227–239

  54. Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl FP (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytol 188:437–450

  55. Pellegrino G, Bellusci F, Musacchio A (2010) Strong post-pollination pre-zygotic isolation between sympatric food-deceptive Mediterranean orchids. Sex Plant Reprod 23:281–289

  56. Pyke GH (1991) What does it cost a plant to produce floral nectar? Nature 350:58–59

  57. Rahme J, Wismer A, Karrenberg S (2009) Pollen competition as an asymmetric reproductive barrier between two closely related Silene species. J Evol Biol 22:1937–1943

  58. Ramsey J, Bradshaw HD Jr, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534

  59. Rieseberg LH, Desrochers AM, Youn ST (1995) Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Am J Bot 82:515–519

  60. Schemske DW (1981) Floral convergence and pollinator sharing in two bee-pollinated tropical herbs. Ecology 62:946–954

  61. Schemske DW (2010) Adaptation and the origin of species. Am Nat 176:S4–S25

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

  63. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

  64. Searcy KB, MacNair MR (1990) Differential seed production in Mimulus guttatus in response to increasing concentrations of copper in the pistil by pollen from copper tolerant and sensitive sources. Evolution 44:1424–1435

  65. Smith SD, Hall SJ, Izquierdo PR, Baum DA (2008) Comparative pollination biology of sympatric and allopatric Andean Iochroma (Solanaceae). Ann Missouri Bot Gard 95:600–617

  66. Sobel JM (2010) Speciation in the western North American wildflower genus Mimulus. Dissertation, Michigan State University

  67. Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64:295–315

  68. Specht CD, Kress WJ, Stevenson DW, DeSalle R (2001) A molecular phylogeny of Costaceae (Zingiberales). Mol Phylogenet Evol 21:333–345

  69. Svensson EI, Eroukhmanoff F, Friberg M (2006) Effects of natural and sexual selection on adaptive population divergence and premating isolation in a damselfly. Evolution 60:1242–1253

  70. Takami Y, Nagata N, Sasabe M, Sota T (2007) Asymmetry in reproductive isolation and its effect on directional mitochondrial introgression in the parapatric ground beetles Carabus yamato and C. albrechti. Popul Ecol 49:337–346

  71. Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. J Ecol 74:329–341

  72. Wang J, Cruzan MB (1998) Interspecific mating in the Piriqueta caroliniana (Turneraceae) complex: effects of pollen load size and composition. Am J Bot 85:1172–1179

  73. Waser NM (1986) Flower constancy: definition, cause, and measurement. Am Nat 127:593–603

  74. Wesselingh RA, Arnold ML (2000) Pollinator behaviour and the evolution of Louisiana iris hybrid zones. J Evol Biol 13:171–180

  75. Whiteman HH, Semlitsch RD (2005) Asymmetric reproductive isolation among polymorphic salamanders. Biol J Linn Soc 86:265–281

  76. Wikelski M, Moxley J, Eaton-Mordas A, Lopez-Uribe MM, Holland R, Moskowitz D, Roubik DW, Kays R (2010) Lange-range movements of Neotropical orchid bees observed via radio telemetry. PLoS ONE 5:e10738. doi:10.1371/journal.pone.0010738

  77. Williams EG, Rouse JL (1990) Relationships of pollen size, pistil length and pollen tube growth rates in Rhododendron and their influence on hybridization. Sex Plant Reprod 3:7–17

  78. Yang C-F, Gituru RW, Guo Y-K (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 90:37–48

  79. Yost JM, Kay KM (2009) The evolution of postpollination reproductive isolation in Costus. Sex Plant Reprod 22:247–255

  80. Zimmerman M, Pyke GH (1988) Experimental manipulations of Polemonium foliosissimum: effects of subsequent nectar production, seed production and growth. J Ecol 76:777–789

  81. Zimmermann Y, Roubik DW, Eltz T (2006) Species-specific attraction to pheromonal analogues in orchid bees. Behav Ecol Sociobiol 60:833–843

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I am grateful to D.W. Schemske for his advice, generosity, and support throughout all parts of this project. I also thank J. Conner, K. Gross, E. A. Herre, K. M. Kay, J. Lau, H. A. Lessios, J. M. Sobel, and two anonymous reviewers for useful comments and suggestions, E. Dittmar, L. Watt and C-Y Yeh for helpful editing, A. González and L. Jiménez for field assistance, S. Carpenter, R. Fuller, M. Hammond for greenhouse management, L. Petroff for developing AFLP markers, and K. Richardson for conducting AFLP. I gratefully acknowledge generous logistical and financial support from the Smithsonian Tropical Research Institute. Data were collected under an Especial permit SE/AP-6-07 and SE/AP-6-08 from Autoridad Nacional del Ambiente and unnumbered permit from Autoridad del Canal de Panamá. I also thank the Department of Plant Biology, Genomics Technology Support Facility, the Graduate School, and the College of Natural Sciences at Michigan State University for additional support for data collection and manuscript preparation.

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Correspondence to Grace F. Chen.

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Communicated by Scott Russell.

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Chen, G.F. Sexual isolation in two bee-pollinated Costus (Costaceae). Plant Reprod 26, 3–16 (2013) doi:10.1007/s00497-012-0203-6

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  • Gametic isolation
  • Floral mechanical isolation
  • Parapatric distribution
  • Pollinator isolation
  • Reproductive isolation
  • Speciation