Skip to main content
SpringerLink
Log in

Increased divergence in floral morphology strongly reduces gene flow in sympatric sexually deceptive orchids with the same pollinator

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

Abstract

In sexually deceptive orchids, pollinator specificity is the main factor responsible for species isolation. The two sexually deceptive orchids Ophrys chestermanii and Ophrys normanii occur sympatrically on Sardinia and attract the same pollinator, males of Bombus vestalis, by producing the same odour bouquets. Since gene flow between these two species has been shown to be almost absent, their genetic distinctness seems to be preserved by other forms of reproductive barrier than pollinator specificity. The aim of this study is to investigate the nature and strength of these isolation barriers which apparently halt gene flow between these two orchids that share the same pollinator. Morphological measurements, combined with observations of cross-pseudocopulations, revealed that, in sympatry, the longer caudicles of O. normanii and the smaller and differently shaped stigmatic cavity in O. chestermanii are the main factors preventing gene flow between these two sympatric species. In contrast, other pre- or post-mating barriers seem to be weak or absent, as the two species have overlapping flowering time and we were able to rear hybrid offspring from interspecific manual crosses. At the same time, genetic analysis of orchid plantlets collected at sympatric sites detected the presence of only two putative hybrid individuals. Thus, the probability of natural cross-pollination between O. normanii and O. chestermanii seems to be strongly limited by divergence in their floral morphology. For some traits, this divergence was found increased between sympatric populations.

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

Access this article

Log in via an institution

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

  • Aceto S, Caputo P, Cozzolino S, Gaudio L, Moretti A (1999) Phylogeny and evolution of Orchis and allied genera based on ITS DNA variation: morphological gaps and molecular continuity. Mol Phylogenetic Evol 13:67–76

    Article  CAS  Google Scholar 

  • Agren L, Kullenberg B, Sensenbaugh T (1984) Congruences in pilosity between 3 species of Ophrys Orchidaceae and their hymenopteran pollinators. Nova acta Regiae Societatis Scientiarum Upsaliensis Ser. V C 3:15–25

    Google Scholar 

  • Ascensao L, Francisco A, Cotrim H, Pais MS (2005) Comparative structure of the labellum in Ophrys fusca and O. lutea (Orchidaceae). Am J Bot 92:1059–1067

    Article  PubMed  Google Scholar 

  • Ayasse M (2006) Floral scent and pollinator attraction in sexually deceptive orchids. In: Dudareva N, Pickersky E (eds) Biology of floral scent. CRC Press, Boca Raton, pp 219–241

    Chapter  Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006

    Article  CAS  PubMed  Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Ibarra F, Francke W (2003) Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proc R Soc B Biol Sci 270:517–522

    Article  CAS  Google Scholar 

  • Ayasse M, Stökl J, Francke W (2011) Chemical ecology and speciation in sexually deceptive orchids. Phytochemistry 72:1667–1677

    Article  CAS  PubMed  Google Scholar 

  • Beyrle H, Penningsfeld F, Hock B (1989) Mykorrhiza-Synthese in gärtnerischen Kultursubstraten und in natürlichen Böden. Die Orchidee 4:173–177

    Google Scholar 

  • Borg-Karlson AK (1990) Chemical and ethological studies of pollination in the genus Ophrys (Orchidaceae). Phytochemistry 29:1359–1387

    Article  CAS  Google Scholar 

  • Breitkopf H, Onstein RE, Cafasso D, Schlüter PM, Cozzolino S (2014) Multiple shifts to different pollinators fuelled rapid diversification in sexually deceptive Ophrys orchids. New Phytol. doi:10.1111/nph.13219

    PubMed  Google Scholar 

  • Cafasso D, Widmer A, Cozzolino S (2005) Chloroplast DNA inheritance in the orchid Anacamptis palustris using single-seed polymerase chain reaction. J Hered 96:66–70

    Article  CAS  PubMed  Google Scholar 

  • Cortis P, Vereecken NJ, Schiestl FP, Lumaga MRB, Scrugli A, Cozzolino S (2009) Pollinator convergence and the nature of species boundaries in sympatric Sardinian Ophrys (Orchidaceae). Ann Bot 104:497–506

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Cozzolino S, Scopece G (2008) Specificity in pollination and consequences for post-mating reproductive isolation in deceptive Mediterranean orchids. Philos Trans R Soc B 363:3037–3046

    Article  Google Scholar 

  • Delforge P (2006) Orchids of Europe, North Africa and the Middle East. A&C Black, London

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Ehrendorfer F (1980) Hybridisierung, Polyploidie und Evolution bei europäisch-mediterranen Orchideen. Die Orchidee Sonderheft 33:15–34

  • Gill DE (1989) Fruiting failure, pollination inefficiency, and speciation in orchids. In: Otte D, Endler JA (eds) Speciation and its consequences. Academy of Natural Science Publications, Philadelphia, pp 458–481

    Google Scholar 

  • Gögler J, Stökl J, Sramkova A, Twele R, Francke W, Cozzolino S, Cortis P, Scrugli A, Ayasse M (2009) Ménage à trois—two endemic species of deceptive orchids and one pollinator. Evolution 63:2222–2234

    Article  PubMed  Google Scholar 

  • Grant V (1971) Plant speciation. Columbia University Press, New York

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harrison RG (1993) Hybrid zones—natural laboratories for evolutionary studies. Trends Ecol Evol 3:158–167

    Google Scholar 

  • Hopkins R (2013) Reinforcement in plants. New Phytol 197:1013–1095

    Article  Google Scholar 

  • Hopkins R, Rausher MD (2012) Pollinator-mediated selection on flower color allele drives reinforcement. Science 335:1090–1092

    Article  CAS  PubMed  Google Scholar 

  • Huang SQ, Shi XQ (2013) Floral isolation in Pedicularis: How do congeners with shared pollinators minimize reproductive interference? New Phytol 199:858–865

    Article  PubMed  Google Scholar 

  • Kullenberg B (1961) Studies in Ophrys pollination. Zoologiska bidrag fran Uppsala 34:1–340

    Google Scholar 

  • Levin DA (1985) Reproductive character displacement in Phlox. Evolution 39:1275–1281

    Article  Google Scholar 

  • Levin DA, Anderson WW (1970) Competition for pollinators between simultaneously flowering species. Am Nat 104:455–467

    Article  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 

  • Norton NA, Fernando MTR, Herlihy CR, Busch JW (2015) Reproductive character displacement shapes a spatially structured petal color polymorphism in Leavenworthia stylosa. Evolution. doi:10.1111/evo.12659

    PubMed  Google Scholar 

  • Paulus HF, Gack C (1990) Pollinators as prepollinating isolation factors: evolution and speciation in Ophrys (Orchidaceae). Isr J Bot 39:43–79

    Google Scholar 

  • Pauw A (2013) Can pollination niches facilitate plant coexistence? Trends Ecol Evol 28:30–37

    Article  PubMed  Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358

    Article  PubMed  Google Scholar 

  • Schemske DW (2000) Understanding the origin of species. Evolution 54:1069–1073

    Article  Google Scholar 

  • Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264

    Article  CAS  PubMed  Google Scholar 

  • Schiestl FP, Ayasse M (2000) Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior. Behav Ecol Sociobiol 48:303–307

    Article  Google Scholar 

  • Schiestl FP, Ayasse M (2002) Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Syst Evol 234:111–119

    Article  CAS  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422

    Article  CAS  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, Widmer A, Cozzolino S (2008) Evolution of postzygotic reproductive isolation in a guild of deceptive orchids. Am Nat 171:315–326

    Article  PubMed  Google Scholar 

  • Slatkin M (1980) Ecological character displacement. Ecology 61:163–177

    Article  Google Scholar 

  • Smith RA, Rausher MD (2008) Selection for character displacement is constrained by the genetic architecture of floral traits in the ivyleaf morning glory. Evolution 62:2829–2841

    Article  PubMed  Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold, London

    Google Scholar 

  • Stebbins GL, Ferlan L (1956) Population variability, hybridization introgression in some species of Ophrys. Evolution 10:32–46

    Article  Google Scholar 

  • Stökl J, Paulus H, Dafni A, Schulz C, Francke W, Ayasse M (2005) Pollinator attracting odour signals in sexually deceptive orchids of the Ophrys fusca group. Plant Syst Evol 254:105–120

    Article  Google Scholar 

  • Stökl J, Twele R, Erdmann DH, Francke W, Ayasse M (2007) Comparison of the flower scent of the sexually deceptive orchid Ophrys iricolor and the female sex pheromone of its pollinator Andrena morio. Chemoecology 17:231–233

    Article  Google Scholar 

  • Stökl J, Schlüter PM, Stuessy TF, Paulus HF, Assum G, Ayasse M (2008) Scent variation and hybridization cause the displacement of a sexually deceptive orchid species. Am J Bot 95:472–481

    Article  PubMed  Google Scholar 

  • Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN (2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol J Linn Soc Lond 84:1–54

    Article  Google Scholar 

  • van der Niet T, Johnson SD (2012) Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol Evol 27:353–361

    Article  PubMed  Google Scholar 

  • Vereecken NJ, Cozzolino S, Schiestl FP (2010) Hybrid floral novelty drives pollinator shift in sexually deceptive orchids. BMC Evol Biol 10:103

    Article  PubMed Central  PubMed  Google Scholar 

  • Warcup JH (1973) Symbiotic germination of some Australian terrestrial orchids. New Phytol 72:387–392

    Article  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 

  • Xu S, Schlüter PM, Scopece G, Breitkopf H, Gross K, Cozzolino S, Schiestl FP (2011) Floral isolation is the main reproductive barrier among closely related sexually deceptive orchids. Evolution 65:2606–2620

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Schlüter PM, Schiestl FP (2012) Pollinator-driven speciation in sexually deceptive orchids. Int J Ecol 285081:9

    Google Scholar 

Download references

Acknowledgments

We thank Claudia Gack, Manfred Kalteisen, Cesario Giotta and Marcello Piccitto for helping us to collect plant material and Hannes Paulus, Hannah Burger and Heiko Bellmann for their help in producing figures. Financial support by the German Science Foundation (AY12/1-1, AY12/1-2) and the FAZIT-Stiftung is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Institute for Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069, Ulm, Germany

    Julia Gögler & Manfred Ayasse

  2. Institute of Zoology, University of Regensburg, Universitätsstraße 31, 93053, Regensburg, Germany

    Johannes Stökl

  3. Department of Life and Environmental Sciences, University of Cagliari, Viale S. Ignazio 13, 09123, Cagliari, Italy

    Pierluigi Cortis

  4. Myorchids Ltd., Lindenmahdstr. 19, 86382, Stadtbergen, Germany

    Heinrich Beyrle

  5. Department of Biology, University of Naples Federico II, Via Cinthia, 80126, Naples, Italy

    Maria Rosaria Barone Lumaga & Salvatore Cozzolino

Authors
  1. Julia Gögler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johannes Stökl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierluigi Cortis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Heinrich Beyrle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Rosaria Barone Lumaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Salvatore Cozzolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manfred Ayasse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Salvatore Cozzolino.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary video 1: B. vestalis male, carrying pollinaria of O. normanii, pseudocopulating with a flower of O. chestermanii. It could be noted that the O. normanii pollinaria do not fit into the small stigmatic cavity of O. chestermanii. (WMV 1069 kb)

Supplementary video 2: B. vestalis male, carrying pollinaria of O. normanii, pseudocopulating with a flower of O. normanii. It could be noted that the O. normanii pollinaria well fit into the large stigmatic cavity of O. normanii. (WMV 1588 kb)

10682_2015_9779_MOESM3_ESM.tif

Supplementary Fig. 1: SEM images of stigmatic cavity of O. normanii (left) and O. chestermanii (right) (bar = 1 mm). (TIFF 4522 kb)

10682_2015_9779_MOESM4_ESM.tif

Supplementary Fig. 2: Frontal details of stigmatic cavities of flowers from three individuals of allopatric O. normanii (a–c), sympatric O. normanii (d–f), sympatric O. chestermanii (g–i), close allopatric O. chestermanii (j–l) and far allopatric O. chestermanii (m–o). (TIFF 15209 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gögler, J., Stökl, J., Cortis, P. et al. Increased divergence in floral morphology strongly reduces gene flow in sympatric sexually deceptive orchids with the same pollinator. Evol Ecol 29, 703–717 (2015). https://doi.org/10.1007/s10682-015-9779-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-015-9779-2

Keywords

Search

Navigation