Pollinator specificity drives strong prepollination reproductive isolation in sympatric sexually deceptive orchids

Evolution

Volumn 68, Issue 6, 2014, Pages 1561-1575

  Whitehead, Michael R ^a   Peakall, Rod ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Chiloglottis; Floral isolation; Floral odor; Hybridization; Pollinator isolation; Population genetics; Prezygotic isolation; Reproductive isolation; Sexual deception

Indexed keywords

FLORAL TRAIT; HYBRIDIZATION; MONOCOTYLEDON; ODOR; POLLINATOR; POPULATION GENETICS; REPRODUCTIVE ISOLATION; SYMPATRY;

CHILOGLOTTIS; CHILOGLOTTIS VALIDA; ORCHIDACEAE;

ESSENTIAL OIL;

ANIMAL; CHEMISTRY; CHLOROPLAST GENE; FLOWER; GENETICS; HETEROSIS; HYBRIDIZATION; ORCHIDACEAE; PHYSIOLOGY; PLANT GENE; POLLINATION; REPRODUCTIVE ISOLATION; SYMPATRY; WASP;

ANIMALS; FLOWERS; GENES, CHLOROPLAST; GENES, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; OILS, VOLATILE; ORCHIDACEAE; POLLINATION; REPRODUCTIVE ISOLATION; SYMPATRY; WASPS;

EID: 84901692620     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12382     Document Type: Article

References (71)

1. Anderson, E. C., and E. A. Thompson. 2002. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217-1229.
2. Ayasse, M., J. Stökl, and W. Francke. 2011. Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72:1667-1677.
3. Bandelt, H. J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16:37-48.
4. Banks, S. C., and R. Peakall. 2012. Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol. Ecol. 21:2092-2105.
5. Batty, A. L., K. W. Dixon, M. Brundrett, and K. Sivasithamparam. 2001. Constraints to symbiotic germination of terrestrial orchid seed in a mediterranean bushland. New Phytol. 152:511-520.
6. Burgarella, C., Z. Lorenzo, R. Jabbour-Zahab, R. Lumaret, E. Guichoux, R. J. Petit, A. Soto, and L. Gil. 2009. Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 102:442-452.
7. Chari, J., and P. Wilson. 2001. Factors limiting hybridization between Penstemon spectabilis and Penstemon centranthifolius. Can. J. Bot. 79:1439-1448.
8. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43:362-381.
9. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.
10. Darwin, C. R. 1877. The various contrivances by which orchids are fertilised by insects. John Murray, Lond.
11. Dell'Olivo, A., M. E. Hoballah, T. Gübitz, and C. Kuhlemeier. 2011. Isolation barriers between Petunia axillaris and Petunia integrifolia (Solanaceae). Evolution 65:1979-1991.
12. Dobzhansky, T. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
13. Ebert, D., and R. Peakall. 2009. Chloroplast simple sequence repeats (cpSSRs): technical resources and recommendations for expanding cpSSR discovery and applications to a wide array of plant species. Mol. Ecol. Res. 9:673-690.
14. Ebert, D., C. Hayes, and R. Peakall. 2009. Chloroplast simple sequence repeat markers for evolutionary studies in the sexually deceptive orchid genus Chiloglottis. Mol. Ecol. Res. 9:784-789.
15. Ellis, A. G., and S. D. Johnson. 2010. Floral mimicry enhances pollen export: the evolution of pollination by sexual deceit outside of the Orchidaceae. Am. Nat. 176:E143-E151.
16. Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes-application to human mitochondrial-DNA restriction data. Genetics 131:479-491.
17. Flanagan, N. S., D. Ebert, C. Porter, M. Rossetto, and R. Peakall. 2006. Microsatellite markers for evolutionary studies in the sexually deceptive orchid genus Chiloglottis. Mol. Ecol. Notes 6:123-126.
18. Fluxus Technology Ltd. 2010. Network 4.6.0.0. Available at http://www.fluxus-engineering.com/.
19. Forster, P., A. Röhl, P. Lünnemann, C. Brinkmann, T. Zerjal, C. Tyler-Smith, and B. Brinkmann. 2000. A short tandem repeat-based phylogeny for the human Y chromosome. Am. J. Hum. Genet. 67:182-196.
20. Franke, S., F. Ibarra, C. M. Schulz, R. Twelle, J. Poldy, R. A. Barrow, R. Peakall, F. P. Schiestl, and W. Francke. 2009. The discovery of 2, 5-dialkylcyclohexan-1, 3-diones as a new class of natural products. Proc. Natl. Acad. Sci. USA 106:8877-8882.
21. Gaskett, A. C. 2011. Orchid pollination by sexual deception: pollinator perspectives. Biol. Rev. 86:33-75.
22. Grant, V. 1949. Pollination systems as isoltaing mechanisms in angiosperms. Evolution 3:82-97.
23. Griffiths, K. E., J. W. H. Trueman, G. R. Brown, and R. Peakall. 2011. Molecular genetic analysis and ecological evidence reveals multiple cryptic species among thynnine wasp pollinators of sexually deceptive orchids. Mol. Phylogenet. Evol. 59:195-205.
24. Hodges, S. A., and M. L. Arnold. 1994. Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. Proc. Natl. Acad. Sci. USA 91:2493-2496.
25. Husband, B. C., and H. A. Sabara. 2004. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol. 161:703-713.
26. Jewell, C., A. D. Papineau, R. Freyre, and L. C. Moyle. 2012. Patterns of reproductive isolation in Nolana (Chilean bellflower). Evolution 66:2628-2636.
27. Johnson, S. D. 2006. Pollinator-driven speciation in plants. Pp. 295-310 in L. D. Harder and S. C. H. Barrett, eds. Ecology and evolution of flowers. Oxford Univ. Press, New York.
28. Kay, K. M. 2006. Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:538-552.
29. Linde, C. C., R. D. Phillips, M. D. Crisp, and R. Peakall. 2014. Congruent species delineation of Tulasnella using multiple loci and methods. New Phytol. 201:6-12.
30. Lowry, D. B., J. L. Modliszewski, K. M. Wright, C. A. Wu, and J. H. Willis. 2008. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. B Biol. Sci. 363:3009-3021.
31. Marks, G. E. 1954. An aceto-carmine glycerol jelly for use in pollen-fertility counts. Stain Technol. 29:277.
32. Martin, N. H., and J. H. Willis. 2007. Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68-82.
33. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York.
34. Meirmans, P. G. 2006. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399-2402.
35. Milne, R. I., S. Terzioglu, and R. J. Abbott. 2003. A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol. Ecol. 12:2719-2729.
36. Morrison, D. A., M. McDonald, P. Bankoff, P. Quirico, and D. Mackay. 1994. Reproductive isolation mechanisms among four closely-related species of Conospermum (Proteaceae). Bot. J. Linn. Soc. 116:13-31.
37. Moyle, L. C., M. S. Olson, and P. Tiffin. 2004. Patterns of reproductive isolation in three Angiosperm genera. Evolution 58:1195-1208.
38. Peakall, R. 2007. Speciation in the Orchidaceae: confronting the challenges. Mol. Ecol. 16:2834-2837.
39. Peakall, R., and P. E. Smouse. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288-295.
40. Peakall, R., and P. E. Smouse. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetics software for teaching and research-an update. Bioinformatics 28: 2537-2539.
41. Peakall R., and M. R. Whitehead. 2014. Floral odour chemistry defines species boundaries and underpins strong reproductive isolation in sexually deceptive orchids. Ann. Bot. 113:341-355.
42. Peakall, R., P. E. Smouse, and D. R. Huff. 1995. Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloe dactyloides. Mol. Ecol. 4:135-147.
43. Peakall, R., C. C. Bower, A. E. Logan, and H. I. Nicol. 1997. Confirmation of the hybrid origin of Chiloglottis x pescottiana (Orchidaceae: Diurideae). 1. Genetic and morphometric evidence. Aust. J. Bot. 45:839-855.
44. Peakall, R., D. Ebert, J. Poldy, R. Barrow, W. Francke, C. Bower, and F. Schiestl. 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.
45. Phillips, R. D., K. W. Dixon, and R. Peakall. 2012. Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family. Mol. Ecol. 21:5208-5220.
46. Phillips, R. D., D. Scaccabarozzi, B. A. Retter, C. Hayes, G. R. Brown, K. W. Dixon, and R. Peakall. 2014. Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Ann. Bot. In press. doi: 10.1093/aob/mct295.
47. Poldy, J., R. Peakall, and R. A. Barrow. 2008. Pheromones and analogs from Neozeleboria wasps and the orchids that seduce them: a versatile synthesis of 2, 5-dialkylated 1, 3-cyclohexanediones. Tetrahedron Lett. 49:2446-2449.
48. Poldy, J., R. Peakall, and R. A. Barrow. 2009. Synthesis of chiloglottones-semiochemicals from sexually deceptive orchids and their pollinators. Org. Biomol. Chem. 7:4296-4300.
49. Ramsey, J., H. D. Bradshaw, and D. W. Schemske. 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520-1534.
50. Rieseberg, L., and J. Willis. 2007. Plant speciation. Science 317:910-914.
51. Roche, S. A., R. J. Carter, R. Peakall, L. M. Smith, M. R. Whitehead, and C. C. Linde. 2010. A narrow group of monophyletic Tulasnella (Tulasnellaceae) symbiont lineages are associated with multiple species of Chiloglottis (Orchidaceae): implications for orchid diversity. Am. J. Bot. 97:1313-1327.
52. Schiestl, F. P. 2005. On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255-264.
53. Schiestl, F. P., and R. Peakall. 2005. Two orchids attract different pollinators with the same floral odor compound: ecological and evolutionary implications. Funct. Ecol. 19:674-680.
54. Schiestl, F. P., and P. M. Schluter. 2009. Floral isolation, specialized pollination, and pollinator behavior in orchids. Ann. Rev. Entomol. 54:425-446.
55. Schiestl, F. P., M. Ayasse, H. F. Paulus, C. Lofstedt, B. S. Hansson, F. Ibarra, and W. Francke. 1999. Orchid pollination by sexual swindle. Nature 399:421-422.
56. Schiestl, F. P., R. Peakall, J. G. Mant, F. Ibarra, C. Schulz, S. Franke, and W. Francke. 2003. The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437-438.
57. Scopece, G., A. Musacchio, A. Widmer, and S. Cozzolino. 2007. Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61:2623-2642.
58. Scopece, G., A. Croce, C. Lexer, and S. Cozzolino. 2013. Components of reproductive isolation between Orchis mascula and Orchis pauciflora. Evolution 67:2083-2093.
59. Stebbins, G. L. 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Ann. Rev. Ecol. Syst. 1:307-326.
60. Swarts, N. D., E. A. Sinclair, A. Francis, and K. W. Dixon. 2010. Ecological specialization in mycorrhizal symbiosis leads to rarity in an endangered orchid. Mol. Ecol. 19:3226-3242.
61. Taylor, S. J., M. Arnold, and N. H. Martin. 2009. The genetic architecture of reproductive isolation in Louisiana Irises: hybrid fitness in nature. Evolution 63:2581-2594.
62. Tremblay, R. L., J. D. Ackerman, J. K. Zimmerman, and R. N. Calvo. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol. J. Linn. Soc. 84:1-54.
63. Vähä, J.-P., and C. R. Primmer. 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 15:63-72.
64. van der Niet, T., and S. D. Johnson. 2012. Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol. Evol. 27:353-361.
65. Van der Niet, T., R. Peakall, and S. D. Johnson. 2014. Pollinator-driven, ecological speciation in plants: new evidence and future perspectives. Ann. Bot. 113:199-211.
66. Vereecken, N. J., C. A. Wilson, S. Hötling, S. Schulz, S. A. Banketov, and P. Mardulyn. 2012. Pre-adaptations and the evolution of pollination by sexual deception: Cope's rule of specialization revisited. Proc. R. Soc. B Biol. Sci. 279:4786-4794.
67. Whitehead, M. R. 2012. The evolutionary biology of pollination: studies in an Australian genus of sexually deceptive orchids. Ph.D. thesis, The Australian National University, Canberra, Australia. Available at http://hdl.handle.net/1885/10260.
68. Whitehead, M. R., and R. Peakall. 2009. Integrating floral scent, pollination ecology and population genetics. Funct. Ecol. 23:863-874.
69. Widmer, A., C. Lexer, and S. Cozzolino. 2008. Evolution of reproductive isolation in plants. Heredity 102:31-38.
70. Xu, S., P. M. Schlüter, U. Grossniklaus, and F. P. Schiestl. 2012. The genetic basis of pollinator adaptation in a sexually deceptive orchid. PLoS Genet. 8:e1002889.
71. Xu, S. Q., P. M. Schluter, G. Scopece, H. Breitkopf, K. Gross, S. Cozzolino, and F. P. Schiestl. 2011. Floral isolation is the main reproductive barrier among closely related sexually deceptive orchids. Evolution 65:2606-2620.