Skip to main content
Log in

Pollinators and crossability as reproductive isolation barriers in two sympatric oil-rewarding Calceolaria (Calceolariaceae) species

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Pollinator species are widely accepted as an important factor in plant reproductive isolation. Although mostly investigated in plants visited by different groups of pollinators (e.g., hummingbirds vs bees), few studies have examined the role of pollinators belonging to the same taxonomic group (e.g., only bees) on plant reproductive isolation. In this study, we investigate this question by evaluating pre- and post-zygotic mechanisms putatively involved in the reproductive isolation of two oil-rewarding sympatric Calceolaria species (i.e., Calceolaria filicaulis and C. arachnoidea) in an Andean ecosystem of Chile. We estimated reproductive isolation values using a combination of field (pollinator visitation rates) and experimental (intra and interspecific manual cross-pollination and seed germination of parents and hybrids) evidence. The two Calceolaria species were preferentially visited by different oil-collecting bee species. Results from hand cross-pollination experiments indicate that intraspecific crossings produced significantly more seeds than interspecific ones. Notwithstanding, seed germination essays did not reveal differences between parental and hybrids. Taken together, these results suggest that pollinator species are responsible for most of the reproductive isolation in the two Calceolaria species studied here. This study is the first assessment of pollinator-mediated reproductive isolation in Calceolaria species and the first to document reproductive barriers in oil-rewarding plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aldriege G, Campbell DR (2006) Asymmetrical pollen success in Ipomopsis (Polemoniaceae) contact sites. Am J Bot 93:903–909

    Article  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Bischoff M, Raguso RA, Jürgens A et al (2015) Context-dependent reproductive isolation mediated by floral scent and color. Evolution 69(1):1–13

    Article  PubMed  Google Scholar 

  • Burke JM, Shanna E, Arnold ML (1998) Hybrid fitness in the Lousiana irises: analysis of parental and F1 performance. Evolution 52:37–43

    PubMed  Google Scholar 

  • Byers K, Vela J, Peng F et al (2014) Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkey flowers (Mimulus). Plant J 80(6):1031–1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell DR, Alarcón R, Wu CA (2003) Reproductive isolation and hybrid pollen disadvantage in Ipomopsis. J Evol Biol 16:536–540

    Article  CAS  PubMed  Google Scholar 

  • Carrió E, Güemes J (2014) The effectiveness of pre- and post-zygotic barriers in avoiding hybridization between two snapdragons (Antirrhinum L.: Plantaginaceae). Bot J Linn Soc 176:159–172

    Google Scholar 

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

    Google Scholar 

  • Cosacov A, Sérsic A, Sosa V, De-Nova A et al (2009) New insights into the phylogenetic relationships, character evolution, and phylogeographic patterns of Calceolaria (Calceolariaceae). Am J Bot 96:2240–2255

    Article  PubMed  Google Scholar 

  • Costa C, Lambert S, Borba EL, Paganucci L (2007) Post-zygotic reproductive isolation between sympatric taxa in the Chamaecrista desvauxii complex (Leguminosae-Caesalpinioideae). Ann Bot 99:625–635

    Article  PubMed  PubMed Central  Google Scholar 

  • Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond B 353:287–305

    Article  CAS  Google Scholar 

  • 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 144:471–478

    Article  Google Scholar 

  • Ehrhart C (2000) Die Gattung Calceolaria (Scrophulariaceae) in Chile. Bibliotheca Bot 153:1–283

    Google Scholar 

  • Emms SK, Hodges SA, Arnold ML (1996) Pollen-tube competition, siring success and consistent asymmetric hybridization in Louisiana irises. Evolution 50:2201–2206

    Article  PubMed  Google Scholar 

  • Escobar F, Aceituno P (1988) Influencia del fenómeno ENSO sobre la precipitación nival en el sector andino de Chile central durante el invierno. Bull Inst Fr Estudes Andines 27:753–759

    Google Scholar 

  • Esterio GR, Cares-Suárez R, Salinas P et al (2013) Assessing the impact of the invasive buff-tailed bumblebee (Bombus terrestris) on the pollination of the native Chilean herb Mimulus luteus. Arthropod-Plant Interact 7:467–474

    Article  Google Scholar 

  • Grant V (1949) Pollination systems as isolating mechanisms in angiosperms. Evolution 3:82–97

    Article  CAS  PubMed  Google Scholar 

  • Grant V, Grant KA (1965) Flower pollination in the Phlox family. Columbia University Press, New York

    Google Scholar 

  • Herrera C (1988) variation in mutualisms: the spatio-temporal mosaic of pollinator assemblage. Biol J Linn Soc 35:95–125

    Article  Google Scholar 

  • Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Ann Rev Ecol Syst 30:109–132

    Article  Google Scholar 

  • Husband BC, Schemske DW, Burton TL, Goodwillie C (2002) Pollen competition as a unilateral reproductive barrier between sympatric diploid and teraploid Chamerion angustifolium. Proc R Soc Lond B 269:2565–2571

    Article  Google Scholar 

  • Kay K (2006) Reproductive isolation between two closely related hummingbird-pollinated neotropical gingers. Evolution 60:538–552

    PubMed  Google Scholar 

  • Lowry DB, Modliszewski JL, Wright KM et al (2011) The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosoph Trans R Soc Lond B 363:3009–3021

    Article  Google Scholar 

  • Marqués I, Rossello-Graell A, Draper D, Iriondo JM (2007) Pollination patterns limit hybridization between two sympatric species of Narcissus (Amaryllidaceae). Am J Bot 94:1352–1359

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Medel R, Botto-Mahan C, Kalin-Arroyo M (2003) Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84:1721–1732

    Article  Google Scholar 

  • Molau U (1988) Scrophulariaceae-part I. Calceolarieae. Flora Neotrop 47:1–326

    Google Scholar 

  • Montalva J, Dudley L, Arroyo MK et al (2011) Geographic distribution and associated flora of native and introduced bumblebees (Bombus spp.) in Chile. J Apic Res 50:11–21

    Article  Google Scholar 

  • Murúa M, Espíndola A (2015) Pollination syndromes in a specialized plant-pollinator interaction: does floral morphology predict pollinators in Calceolaria? Plant Biol 17:551–557

    Article  PubMed  Google Scholar 

  • Murúa M, Cisterna J, Rosende B (2014) Pollination ecology and breeding system of two Calceolaria species in Chile. Rev Chil Hist Nat 87:7

    Article  Google Scholar 

  • Olesen J, Bascompte J, Elberling H et al (2008) Temporal dynamics in a pollination network. Ecology 89(6):1573–1582

    Article  PubMed  Google Scholar 

  • Pauw A (2006) Floral syndromes accurately predict pollination by a specialized oil-collecting bee (Rediviva peringueyi, Melittidae) in a guild of South African orchids (Coryciinae). Am J Bot 93(6):917–926

    Article  PubMed  Google Scholar 

  • Petanidou T, Kallimanis A, Tzanopoulos J et al (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications fir estimates of specialization. Ecol Lett 11:564–575

    Article  PubMed  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rasmussen C, Olesen JM (2000) Oil flowers and oil-collecting bees. Det Norske Videnskaps-akademi. I. Matematisk Naturvidenskapelige Klasse. Skrifter Ny serie 39:23–31

    Google Scholar 

  • Schiestl FP, Schlüter PM (2009) Floral isolation, specialized pollination, and pollinator behavior in orchids. Ann Rev Entomol 54:425–446

    Article  CAS  Google Scholar 

  • Schmid-Hempel R, Eckhardt M, Goulson D et al (2014) The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837

    Article  PubMed  Google Scholar 

  • Scopece G, Musacchio A, Widmer A, Cozzolino S (2007) Patterns of reproductive isolation in mediterranean deceptive orchids. Evolution 61:2623–2642

    Article  PubMed  Google Scholar 

  • Scopece G, Croce A, Lexer C, Cozzolino S (2013) Components of reproductive isolation between Orchis mascula and Orchis pauciflora. Evolution 67:2083–2093

    Article  PubMed  Google Scholar 

  • Sedeek K, Scopece G, Staedler Y et al (2014) Genic rather than genome-wide differences between sexually deceptive Ophrys orchids with different pollinators. Mol Ecol 23:6192–6205

    Article  CAS  PubMed  Google Scholar 

  • Sérsic AN (2004) Pollination biology in the genus Calceolaria L. (Calceolariaceae). Stapfia 82:1–121

    Google Scholar 

  • Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms. I: pollination mechanisms. Ann Rev Ecol Syst 1:307–326

    Article  Google Scholar 

  • Tiffin P, Olson MS, Moyle LC (2001) Asymmetrical crossing barriers angiosperms. Proc R Soc Lond B 268:861–867

    Article  CAS  Google Scholar 

  • Wendt T, Ferreira MB, Gelli AP, Iglesias R (2001) Reproductive biology and natural hybridization between two endemic species of Pitcairnia (Bromeliaceae). Am J Bot 88:1760–1767

    Article  CAS  PubMed  Google Scholar 

  • Whitehead MR, Peakall R (2014) Pollinator specificity drives strong prepollination reproductive isolation in sympatric sexually deceptive orchids. Evolution 68:1561–1575

    Article  PubMed  Google Scholar 

  • Widmer A, Lexer C, Cozzolino S (2009) Evolution of reproductive isolation in plants. Heredity 102:31–38

    Article  CAS  PubMed  Google Scholar 

  • Yang C-F, Gituru R-W, Guo Y-H (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

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Jannina Cisterna, Carmen Gloria Ossa, Fabiola Orrego and Isabel Mujica for help with greenhouse experiments, Daniel Caetano and Catalina González for help in data analysis, Fernanda Pérez and Pontificia Universidad Católica de Chile for providing logistic support, and Corporación Nacional Forestal (CONAF) for authorization to work in the National Reserve. This work was supported by Beca de Apoyo a la Realización de la Tesis Doctoral CONICYT [24110094], FONDECYT [PD3150267], FONDECYT [11110120], and FONDECYT [1150112]. AE was supported by the Swiss National Science Foundation (Grant PBNEP3-140192).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maureen Murúa.

Additional information

Anahí Espíndola and Rodrigo Medel: share joint last authorship.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 88 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murúa, M., Espíndola, A., González, A. et al. Pollinators and crossability as reproductive isolation barriers in two sympatric oil-rewarding Calceolaria (Calceolariaceae) species. Evol Ecol 31, 421–434 (2017). https://doi.org/10.1007/s10682-017-9894-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-017-9894-3

Keywords

Navigation