Skip to main content

Sympatric reinforcement of reproductive barriers between Neotinea tridentata and N. ustulata (Orchidaceae)

Abstract

Reinforcement is the process by which selection favors traits that decrease mating between two incipient species in response to costly mating or the production of maladapted hybrids, causing the evolution of greater reproductive isolation between emerging species. I have studied a pair of orchids, Neotinea tridentata and N. ustulata, to examine the level of postmating pre- and post-zygotic isolating mechanisms that maintain these species, and the degree to which the boundary may still be permeable to gene flow. In this study, I performed pollen tube growth rate experiments and I investigated pre- and post-zygotic barriers by performing hand pollination experiments in order to evaluate fruit set, embryonate seed set and seed germination rates by intra- and interspecific crosses. Fruit set, the percentage of embryonate seeds and germinability of interspecific crosses were reduced compared to intraspecific pollinations, showing significant differences between sympatric and allopatric populations. While in allopatric populations the post-pollination isolation index ranged between 0.40 and 0.11, in sympatric populations orchid pairs showed total isolation due to post-pollination prezygotic barriers, guaranteed at the level of pollen–stigma interactions. Indeed, in sympatric populations, pollen tubes reached the ovary after 24 h in only 8 out of 45 plants; in the remaining cases, the pollen tubes did not enter the ovary, and thus no fruit set occurred. This pair of orchids is characterized by postmating pre-zygotic reproductive isolation in sympatric populations that prevents the formation of hybrids. This mechanism of speciation, starting in allopatry and triggering the reinforcement mechanisms of reproductive isolation in secondary sympatry, is the most likely explanation for the pattern of evolutionary transitions found in this pair of orchids.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abbott RJ, Rieseberg LH (2012) Hybrid speciation. Wiley, Chichester

    Book  Google Scholar 

  • Barton NH, Hewitt GM (1981) The genetic basis of hybrid inviability in the grasshopper Podisma pedestris. Heredity 47:367–383

    Article  Google Scholar 

  • Bateman RM, Hollingsworth PM, Preston J, Yi-Bo L, Pridgeon AM, Chase MW (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Bot J Linn Soc 142:1–40

    Article  Google Scholar 

  • Bellusci F, Pellegrino G, Palermo AM, Musacchio A (2010) Crossing barriers between the unrewarding Mediterranean orchids Serapias vomeracea and S. cordigera. Plant Spe Biol 25:68–76

    Article  Google Scholar 

  • Bernardos S (2004) Cytotaxonomic study of some taxa of the subtribe Orchidinae (Orchidoideae, Orchidaceae) from the Iberian Peninsula. Isr J Plant Sci 52:161–170

    Article  Google Scholar 

  • Bogenhard C (1850) Taschenbuch der Flora von Jena. Wilhelm Engelmann, Leipzig

    Google Scholar 

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

    Google Scholar 

  • Cozzolino S, Aceto S, Caputo P, Menale B (1998) Characterization of Orchis × dietrichiana Bogenh., a natural orchid hybrid. Plant Biosyst 132:71–76

    Article  Google Scholar 

  • Delforge P (2005) Guide des Orchidées d’Europe, d’Afrique du Nord et du Proche- Orient. Delachaux et Niestlé, Neuchâtel-Paris

    Google Scholar 

  • D’Emerico S, Cozzolino S, Pellegrino G, Pignone D, Scrugli A (2002) Heterochromatin distribution in selected taxa of the 42-chromosomes Orchis s.l. (Orchidaceae). Caryologia 55:55–62

    Article  Google Scholar 

  • Djordjević V, Tsiftsis S, Jakovljević K, Šinžar-Sekulić J, Vukojičić S (2012) First record of a natural hybrid Neotinea × dietrichiana (Orchidaceae) in Serbia. Phytol Balc 18:163–171

    Google Scholar 

  • Dobzhansky T (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321

    Article  Google Scholar 

  • Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733

    Article  Google Scholar 

  • Gölz P, Reinhard HR (1986) Orchideen in Jugoslawien. Mitt Bl Arbeitskr Heim Orch Baden-Württemberg 18:689–827

    Google Scholar 

  • Grant V (1966) The selective origin of incompatibility barriers in the plant genus Gilia. Am Nat 100:99–118

    Article  Google Scholar 

  • Higashiyama T, Kuroiwa H, Kuroiwa T (2003) Pollen-tube guidance: beacons from the female gametophyte. Curr Opin Plant Biol 6:36–41

    Article  PubMed  Google Scholar 

  • Hopkins R (2013) Reinforcement in plants. New Phytol 197:1095–1103

    Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kretzschmar H, Eccarius W, Dietrich H (2007) The Orchid Genera Anacamptis Orchis and Neotinea. Phylogeny, taxonomy, morphology, biology, distribution, ecology and hybridization. EchinoMedia Verlag, Bürgel

    Google Scholar 

  • Lemmon AR, Kirkpatrick M (2006) Reinforcement and the genetics of hybrid incompatibilities. Genetics 173:1145–1155

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Luca A, Palermo AM, Bellusci F, Pellegrino G (2015) Pollen competition between two sympatric Orchis species (Orchidaceae): the overtaking of conspecific on heterospecific pollen as a reproductive barrier. Plant Biol 17:219–225

    CAS  Article  PubMed  Google Scholar 

  • McNeilly T, Antonovics J (1968) Evolution in closely adjacent plant populations. Barriers to gene flow. Heredity 23:205–218

    Article  Google Scholar 

  • Pellegrino G, Musacchio A, Noce ME, Palermo AM, Widmer A (2005) Reproductive versus floral isolation among morphologically similar Serapias L. species (Orchidaceae). J Hered 96:15–23

    CAS  Article  PubMed  Google Scholar 

  • Pellegrino G, Bellusci F, Musacchio A (2009) Genetic integrity of sympatric hybridising plant species: the case of Orchis italica and O. anthropophora. Plant Biol 11:434–441

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Quart Rev Biol 84:253–276

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Reinhard H, Gölz P, Peter R, Wildermurth H (1991) Die Orchideen der Schweiz und angrenzender Gebiete. Fotorotar, Egg

    Google Scholar 

  • Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Robertson C (1928) Flowers and insects. Lists of visitors of four hundred and fifty-three flowers. Science Press Printing Co, Lancaster

    Book  Google Scholar 

  • Schiestl FP, Dötterl S (2012) The evolution of floral scent and olfactory preferences in pollinators: coevolution or pre-existing bias? Evolution 66:2042–2055

    CAS  Article  PubMed  Google Scholar 

  • Scopece G, Musacchio A, Widmer A, Cozzolino S (2007) Patterns of reproductive isolation in Mediterranean 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 

  • Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol S 34:339–364

    Article  Google Scholar 

  • Silvertown J, Servaes C, Biss P, Macleod D (2005) Reinforcement of reproductive isolation between adjacent populations in the Park Grass Experiment. Heredity 95:198–205

    CAS  Article  PubMed  Google Scholar 

  • Sobel JM, Chen GF (2014) Unification of methods for estimating the strength of reproductive isolation. Evolution 68:1511–1522

    Article  PubMed  Google Scholar 

  • Soó R (1980) Orchis L. In: Tutin TG et al (eds) Flora Europaea. Cambridge University Press, Cambridge, pp 337–342

    Google Scholar 

  • Tsiftsis S, Karagiannakidou V, Tsiripidis I (2007) The orchid flora of East Macedonia (NE Greece). J Eur Orch 39:489–526

    Google Scholar 

  • van der Cingel NA (1995) An Atlas of Orchids Pollination–European Orchids. Balkema, Rotterdam

    Google Scholar 

  • Van der Niet T, Johnson SD, Linder HP (2006) Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60:1596–1601

    Article  PubMed  Google Scholar 

  • Van Waes JM, Derbergh PC (1986) In vitro germination of some Western European orchids. Physiol Plant 67:253–261

    Article  Google Scholar 

  • Vöth W (1984) Echinomyia magnicornis ZETT. Bestäuber von Orchis ustulata L. Die Orchidee 35:189–192

    Google Scholar 

  • Whalen MD (1978) Reproductive character displacement and floral diversity in Solanum section Androceras. Syst Bot 3:77–86

    Article  Google Scholar 

  • Wheeler MJ, Franklin-Tong VE, Franklin FCH (2001) The molecular and genetic basis of pollen–pistil interactions. New Phytol 151:565–584

    CAS  Article  Google Scholar 

  • Zitari A, Scopece G, Helal AN, Widmer A, Cozzolino S (2012) Is floral divergence sufficient to maintain species boundaries upon secondary contact in Mediterranean food-deceptive orchids? Heredity 108:219–228

    CAS  Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Pellegrino.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pellegrino, G. Sympatric reinforcement of reproductive barriers between Neotinea tridentata and N. ustulata (Orchidaceae). J Plant Res 129, 1061–1068 (2016). https://doi.org/10.1007/s10265-016-0855-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-016-0855-7

Keywords

  • Neotinea
  • Orchidaceae
  • Orchids
  • Pollen tube
  • Reinforcement
  • Reproductive barriers