Abstract
Empirical studies of post-pollination barriers to gene flow between recently diverged plant species are important to understand ecological processes underlying speciation. Using greenhouse and common garden experiments, we investigated the strength of post-pollination barriers that restrict or prevent gene flow between two subspecies of Antirrhinum: Antirrhinum majus pseudomajus and A. m. striatum. The two are distributed parapatrically but share the same major pollinators (bumblebees), and form narrow hybrid zone in many areas of southern France and northern Spain where they come into close contact. We assessed the strength and symmetry of mating barriers and their homogeneity among populations by comparing fruit set, seed set and offspring performances between intra- and inter-subspecific crosses performed in parental and hybrid populations. Although all populations showed high levels of self-incompatibility, we found very little evidence for barriers to gene flow once pollen had been transferred to the stigma. We suggest that reproductive isolation in this system mostly involves barriers related to processes occurring before pollination, with little or no role of post-pollination barriers.
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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
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
Banovetz SJ, Scheiner SM (1994) The effects of seed mass and the seed ecology of Coreopsis lanceolata. Am Midl Nat 131:65–74
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510
Campbell DR, Waser NM (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676
Campbell DR, Waser NM, Pederson GT (2002) Predicting patterns of mating and potential hybridization from pollinator behavior. Am Nat 159:438–450
Chittka L, Gumbert A, Kunze J (1997) Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behav Ecol 8:239–249
Clausen J (1951) Stages in the evolution of plant species. Cornell University Press, New York
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland
De Nettancourt D (1977) Incompatibility in angiosperms. Springer-Verlag, Berlin
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
East EM (1940) The distribution of self-fertility in the flowering plants. Proc Am Philos Soc 82:449–517
Fenner M (1985) Seed ecology. Chapman and Hall, New York
Fox J (2002) An R and S-plus Companion to applied regression. Sage, London
Gegear RJ, Laverty TM (2005) Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim Behav 69:939–949
Grant V (1992) Floral isolation between ornithophilous and sphingophilous species of Ipomopsis and Aquilegia. Proc Natl Acad Sci USA 89:11828–11831
Harder LD, Cruzan MB, Thompson JD (1993) Unilateral incompatibility and the effects of interspeccific pollination for Erythronium americanum and Erythronium albidum (Liliaceae). Can J Bot 71:353–358
Hodges SA, Burke JM, Arnold ML (1996) Natural formation of Iris hybrids: experimental evidence on the establishment of hybrid zones. Evolution 50:2504–2509
Ippolito AG, Fernandes W, Holtsford TP (2004) Pollinator preferences for Nicotiana alata, N. forgetiana, and their F1 hybrids. Evolution 58:2634–2644
Johnston JA, Grise DJ, Donovan LA, Arnold ML (2001) Environment-dependent performance and fitness of Iris brevicaulis, I. Fulva (Iridaceae), and hybrids. Am J Bot 88:933–938
Jones KN, Reithel J (2001) Pollinator-mediated selection on flower color polymorphism in experimental populations of Antirrhinum (Scrophulariaceae). Am J Bot 88:447–454
Langlade NB, Feng X, Dransfield T, Copsey L, Hanna AI, Thébaud C, Bangham A, Hudson A, Coen E (2005) Evolution through genetically controlled allometry space. Proc Natl Acad Sci USA 102:10221–10226
Levin DA (1971) The origin of reproductive isolating mechanisms in flowering plants. Taxon 20:91–113
Levin DA (1978) The origin of isolating mechanisms in flowering plants. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary Biology, vol II. Appleton Century Crofts, New York, pp 185–317
Lewis D, Crowe LK (1958) Unilateral interspecific incompatibility in flowering plants. Heredity 12:233–256
Lloret F, Casanovas C, Penuelas J (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629
Mable BK (2004) Polyploidy and self-compatibility: is there an association? New Phytol 162:803–811
Mateu-Andrés I, Segarra-Moragues JG (2004) Reproductive system in the Iberian endangered endemic Antirrhinum valentinum F.Q. (Antirrhineae, Scrophulariaceae): consequences for species conservation. Int J Plant Sci 165:773–778
Mather K (1947) Species crosses in Antirrhinum. I. Genetic isolation of the species majus, glutinosum and orontium. Heredity 1:175–186
Ramsey J, Bradshaw HD, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and Mimulus cardinalis (Phrymaceae). Evolution 57:1520–1534
Rhode JM, Cruzan MB (2005) Contribution of heterosis and epistasis to hybrid fitness. Am Nat 166:E124–E139
Rothmaler W (1956) Taxonomische Monographie der Gattung Antirrhinum. Akademie-Verlag, Berlin
SAS (2000) SAS OnlineDoc® (Version 8). SAS institute, Cary
Sokal RR, Rohlf JF (1995) Biometry, 3rd edn. WH Freeman, New York
Tastard E, Andalo C, Giurfa M, Burrus M, Thébaud C (2008) Flower colour variation across a hybrid zone in Antirrhinum as perceived by bumblebee pollinators. Arthropod Plant Interact 2:237–246
Thompson DM (1988) Systematics of Antirrhinum (Scrophulariaceae) in the New World. Syst Bot Monogr 22:1–142
Tiffin P, Olson MS, Moyle LC (2001) Asymmetrical crossing barriers in angiosperms. Proc R Soc Lond 268:861–867
Torres E, Iriondo JM, Pérez C (2002) Vulnerability and determinant of reproductive success in the narrow endemic Antirrhinum microphyllum (Scrophulariaceae). Am J Bot 89:1171–1179
Venables WN, Ripley BD (1999) Modern Applied Statistics with S-Plus, 3rd edn. Springer, New York
Waser NM (2006) Specialization and generalization in plant-pollinator interactions: a historical perspective. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. The University of Chicago Press, Chicago, pp 3–17
Waser NM, Chittka L, Price MV, Williams N, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:279–296
Westoby M, Jurado E, Leishman M (1992) Comparative evolutionary ecology of seed size. Trends Ecol Evol 7:368–372
Whibley AC, Langlade NB, Andalo C, Hanna AI, Bangham A, Thébaud C, Coen E (2006) Evolutionary paths underlying flower color variation in Antirrhinum. Science 313:963–966
Zwettler D, Vieira CP, Schlötterer C (2002) Polymorphic microsatellites in Antirrhinum (Scrophulariaceae), a genus with low levels of nuclear sequence variability. J Hered 93:217–221
Acknowledgments
We thank L. Mantione, E. Lance, E. Beaudoin, V. Manchon, F. Andalo, E. Tastard, N. Norden, F. Jabot and D. Guery for assistance with crosses, measurements and plant culture; and J. Clobert for permission to work at the CNRS field station in Moulis. We are also grateful to D. Rosenthal, H. de Glanville, P. Sochacki, J. Picotte, L. Copsey, M. Dufaÿ and D. Mckey for constructive comments on a previous draft of the manuscript.
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Andalo, C., Cruzan, M.B., Cazettes, C. et al. Post-pollination barriers do not explain the persistence of two distinct Antirrhinum subspecies with parapatric distribution. Plant Syst Evol 286, 223–234 (2010). https://doi.org/10.1007/s00606-010-0303-4
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DOI: https://doi.org/10.1007/s00606-010-0303-4