Skip to main content
Log in

Strong postzygotic isolation prevents introgression between two hybridizing Neotropical orchids, Epidendrum denticulatum and E. fulgens

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

Abstract

Studies on hybrid zones are essential to understand the origin and evolution of reproductive barriers in plants. To achieve this goal, multidisciplinary approaches are often required to investigate the role of multiple reproductive isolation (RI) mechanisms. For Epidendrum denticulatum and E. fulgens, two Neotropical food-deceptive orchid species, we used molecular, cytogenetic and morphological analyses, experimental crosses and environmental envelope models to assess the strength of the RI and the mechanisms that prevent species collapse when hybridization occurs. Based on genetic assignment tests, hybrids between E. denticulatum and E. fulgens were detected. However, the low frequency of hybrid specimens found, coupled with the high morphological differentiation between parental species, suggested that strong barriers exist to interspecific gene exchange. Indeed, hybrid plants were largely sterile, as determined by meiotic data and crossing experiments. In the hybrid zone studied here, strong postzygotic barriers maintain species integrity, and these RI mechanisms may be also important during early stages of speciation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R et al (2013) Hybridization and speciation. J Evol Biol 26:229–246

    Article  CAS  PubMed  Google Scholar 

  • Ackerman JD, Cuevas AA, Hof D (2011) Are deception-pollinated species more variable than those offering a reward? Plant Syst Evol 293:91–99

    Article  Google Scholar 

  • Almeida AM, Figueiredo RA (2003) Ants visit nectaries of Epidendrum denticulatum (Orchidaceae) in a Brazilian rainforest: effects on herbivory and pollination. Braz J Biol 63:551–558

    Article  CAS  PubMed  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Arnold ML, Ballerini ES, Brothers AN (2011) Hybrid fitness, adaptation and evolutionary diversification: lessons learned from Louisiana Irises. Heredity 108:159–166

    Article  PubMed Central  PubMed  Google Scholar 

  • Assis FNM, Souza BCQ, Medeiros-Neto E, Pinheiro F, Silva AEB, Felix LP (2013) Karyology of the genus Epidendrum (Orchidaceae: Laeliinae) with emphasis on subgenus Amphiglottium and chromosome number variability in Epidendrum secundum. Bot J Linn Soc 172:329–344

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Roehl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bleeker W, Matthies A (2005) Hybrid zones between invasive Rorippa austriaca and native R. sylvestris (Brassicaceae) in Germany: ploidy levels and patterns of fitness in the field. Heredity 94:664–670

    Article  CAS  PubMed  Google Scholar 

  • Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393

    Article  CAS  PubMed  Google Scholar 

  • Braconnot P, Otto-Bliesner B, Harrison S, Joussaume S, Peterchmitt JY, Abe-Ouchi A, Crucifix M, Driesschaert E, Fichefet T, Hewitt CD, Kageyama M, Kitoh A, Laine A, Loutre MF, Marti O, Merkel U, Ramstein G, Valdes P, Weber SL, Yu Y, Zhao Y (2007) Results of PMIP2 coupled simulations of the mid-Holocene and Last Glacial Maximum—part 1: experiments and large-scale features. Clim Past 3:261–277

    Article  Google Scholar 

  • Buerkle CA (2005) Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes 5:684–687

    Article  CAS  Google Scholar 

  • Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH (2000) The likelihood of homoploid hybrid speciation. Heredity 84:441–451

    Article  PubMed  Google Scholar 

  • Buggs RJ, Soltis PS, Soltis DE (2011) Biosystematic relationships and the formation of polyploids. Taxon 60:324–332

    Google Scholar 

  • Caddah MK, Campos T, Zucchi MI, de Souza AP, Bittrich V, do Amaral MDCE (2013) Species boundaries inferred from microsatellite markers in the Kielmeyera coriacea complex (Calophyllaceae) and evidence of asymmetric hybridization. Plant Syst Evol 299:731–741

    Article  Google Scholar 

  • Castro S, Münzbergová Z, Raabová J, Loureiro J (2011) Breeding barriers at a diploid–hexaploid contact zone in Aster amellus. Evol Ecol 25:795–814

    Article  Google Scholar 

  • Cerón-Souza I, Rivera-Ocasio E, Medina E, Jiménez JA, McMillan WO, Bermingham E (2010) Hybridization and introgression in New World red mangroves, Rhizophora (Rhizophoraceae). Am J Bot 97:945–957

    Article  PubMed  Google Scholar 

  • Chung MY, Nason JD, Chung MG (2005) Patterns of hybridization and population genetic structure in the terrestrial orchids Liparis kumokiri and Liparis makinoana (Orchidaceae) in sympatric populations. Mol Ecol 14:4389–4402

    Article  CAS  PubMed  Google Scholar 

  • Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, Chang P, Doney SC, Hack JJ, Henderson TB, Kiehl JT, Large WG, McKenna DS, Santer BD, Smith RD (2006) The community climate system model version 3 (CCSM3). J Clim 19:2122–2143

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Da Conceição LP, Oliveira ALPC, Barbosa LV (2006) Characterization of the species Epidendrum cinnabarinum Salzm. (Epidendroideae: Orchidaceae) occurring in dunas do Abaeté-Salvador, Ba-Brasil. Cytologia 71:125–129

    Article  Google Scholar 

  • Dressler RL (1989) Will the real Epidendrum ibaguense please stand up? Am Orchid Soc Bull 58:796–800

    Google Scholar 

  • Dunsterville GC (1979) Orchids of Venezuela—Epidendrum elongatum. Am Orchid Soc Bull 48:447–454

    Google Scholar 

  • Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25:660–669

    Article  PubMed  Google Scholar 

  • Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49

    Article  Google Scholar 

  • Fuhro D, Araújo AM, Irgang BE (2010) Are there evidences of a complex mimicry system among Asclepias curassavica (Apocynaceae), Epidendrum fulgens (Orchidaceae), and Lantana camara (Verbenaceae) in Southern Brazil? Rev Bras Bot 33:589–598

    Google Scholar 

  • Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc R Soc Lond B Biol Sci 266:2247–2252

    Article  Google Scholar 

  • Hágsater E (1984) Towards an understanding of the genus Epidendrum. In: Tan KW (ed) Proceedings of the 11th world orchid conference, Miami, pp 195–201

  • Hágsater E, Soto-Arenas MA (2005) Epidendrum L. In: Pridgeon AM, Cribb PJ, Chase MW, Rasmussen FN (eds) Genera Orchidacearum: Epidendroideae (part one), vol 4. Oxford University Press, Oxford, pp 236–251

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Husband BC, Sabara HA (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium. New Phytol 161:703–713

    Article  Google Scholar 

  • Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev 81:219–235

    Article  PubMed  Google Scholar 

  • Jewell C, Papineau AD, Freyre R, Moyle LC (2012) Patterns of reproductive isolation in Nolana (Chilean Bellflower). Evolution 66:2628–2636

  • Jørgensen MH, Ehrich D, Schmickl R, Koch MA, Brysting AK (2011) Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae). BMC Evol Biol 11:346

    Article  PubMed Central  PubMed  Google Scholar 

  • Juillet N, Scopece G (2010) Does floral trait variability enhance reproductive success in deceptive orchids? Perspect Plant Ecol Evol Syst 12:317–322

    Article  Google Scholar 

  • Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242

    Article  CAS  PubMed  Google Scholar 

  • Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, Oxford

    Google Scholar 

  • Lorenz-Lemke AP, Maeder G, Muschner VC, Stehmann JR, Bonatto SL, Salzano FM, Freitas LB (2006) Diversity and natural hybridization in a highly endemic species of Petunia (Solanaceae): a molecular and ecological analysis. Mol Ecol 15:4487–4497

    Article  CAS  PubMed  Google Scholar 

  • Marques I, Feliner GN, Draper Munt D, Martins-Loução MA, Aguilar JF (2010) Unraveling cryptic reticulate relationships and the origin of orphan hybrid disjunct populations in Narcissus. Evolution 64:2353–2368

    PubMed  Google Scholar 

  • Marques I, Aguilar JF, Martins-Loução MA, Feliner GN (2012) Spatial–temporal patterns of flowering asynchrony and pollinator fidelity in hybridizing species of Narcissus. Evol Ecol 26:1433–1450

    Article  Google Scholar 

  • Marques I, Draper D, Riofrío L, Naranjo C (2014) Multiple hybridization events, polyploidy and low postmating isolation entangle the evolution of neotropical species of Epidendrum (Orchidaceae). BMC Evol Biol 14:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Biotech Histochem 34:125–128

    Article  CAS  Google Scholar 

  • McKenzie-Gopsill A, Kirk H, Drunen WV, Freeland JR, Dorken ME (2012) No evidence for niche segregation in a North American cattail (Typha) species complex. Ecol Evol 2:952–961

    Article  PubMed Central  PubMed  Google Scholar 

  • Milne RI, Terzioglu S, Abbott RJ (2003) A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol Ecol 12:2719–2729

    Article  CAS  PubMed  Google Scholar 

  • Moccia MD, Widmer A, Cozzolino S (2007) The strength of reproductive isolation in hybridizing food deceptive orchids. Mol Ecol 16:2855–2866

    Article  PubMed  Google Scholar 

  • Moraes AP, Chinaglia M, Palma-Silva C, Pinheiro F (2013) Interploidy hybridization in sympatric zones: the formation of Epidendrum fulgens × E. puniceoluteum hybrids (Epidendroideae, Orchidaceae). Ecol Evol 3:3824–3837

    Article  PubMed Central  PubMed  Google Scholar 

  • Moré M, Amorim FW, Benitez-Vieyra S, Medina AM, Sazima M, Cocucci AA (2012) Armament imbalances: match and mismatch in plant–pollinator traits of highly specialized long-spurred orchids. PLoS One 7:e41878

    Article  PubMed Central  PubMed  Google Scholar 

  • Moyle LC, Olson MS, Tiffin P (2004) Patterns of reproductive isolation in three angiosperm genera. Evolution 58:1195–1208

  • Natalis LC, Wesselingh RA (2013) Parental frequencies and spatial configuration shape bumblebee behavior and floral isolation in hybridizing Rhinanthus. Evolution 67:1692–1705

    Article  PubMed  Google Scholar 

  • Orr HA, Turelli M (2001) The evolution of postzygotic isolation: accumulating Dobzhansky–Muller incompatibilities. Evolution 55:1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Otto-Bliesner BL, Marshall S, Overpeck J, Miller G, Hu A (2006) CAPE Last Interglacial Project Members: simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science 311:1751–1753

    Article  CAS  PubMed  Google Scholar 

  • Palma-Silva C, Wendt T, Pinheiro F, Barbará T, Fay MF, Cozzolino S, Lexer C (2011) Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs. Mol Ecol 20:3185–3201

    Article  CAS  PubMed  Google Scholar 

  • Pavarese G, Tranchida-Lombardo V, Galesi R, D’Emerico S, Casotti R, Cristaudo A, Cozzolino S (2013) When polyploidy and hybridization produce a fuzzy taxon: the complex origin of the insular neoendemic Neotinea commutata (Orchidaceae). Bot J Linn Soc 173:707–720

    Article  Google Scholar 

  • Pessoa EM, Alves M, Alves-Araújo A, Palma-Silva C, Pinheiro F (2012) Integrating different tools to disentangle species complexes: a case study in Epidendrum (Orchidaceae). Taxon 61:721–734

    Google Scholar 

  • Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393

    Article  PubMed  Google Scholar 

  • Phillips SJ, Dudik M, Schapire RE (2006) Maximum entropy modelling of species geographic distributions. Ecol Model 190:231–259

  • Pinheiro F, Barros F (2007) Epidendrum secundum Jacq. e E. denticulatum Barb. Rodr. (Orchidaceae): caracteres úteis para a sua separação. Hoehnea 34:563–570

    Article  Google Scholar 

  • Pinheiro F, Cozzolino S (2013) Epidendrum (Orchidaceae) as a model system for ecological and evolutionary studies in the Neotropics. Taxon 62:77–88

    Google Scholar 

  • Pinheiro F, Santos MO, Barros F, Meyer D, Salatino A, Souza AP, Cozzolino S (2008a) Isolation and characterization of microsatellite loci in the Brazilian orchid Epidendrum fulgens. Conserv Genet 9:1661–1663

    Article  CAS  Google Scholar 

  • Pinheiro F, Santos MO, Palma-Silva C, Barros F, Meyer D, Salatino A, Souza AP, Cozzolino S (2008b) Isolation and characterization of microsatellite loci in Epidendrum puniceoluteum, an endemic orchid from the Atlantic Rainforest. Mol Ecol Resour 8:1114–1116

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro F, Koehler S, Corrêa AM, Salatino MLF, Salatino A, Barros F (2009a) Phylogenetic relationships and infrageneric classification of Epidendrum subgenus Amphiglottium (Laeliinae, Orchidaceae). Plant Syst Evol 283:165–177

    Article  Google Scholar 

  • Pinheiro F, Palma-Silva C, Barros F, Félix LP, Lexer C, Cozzolino S, Fay MF (2009b) Chloroplast microsatellite markers for the Neotropical orchid genus Epidendrum, and cross-amplification in other Laeliinae species (Orchidaceae). Conserv Genet Resour 1:505–511

    Article  Google Scholar 

  • Pinheiro F, Barros F, Palma-Silva C, Meyer D, Fay MF, Suzuki RM, Lexer C, Cozzolino S (2010) Hybridization and introgression across different ploidy levels in the Neotropical orchids Epidendrum fulgens and E. puniceoluteum (Orchidaceae). Mol Ecol 19:3981–3994

    Article  PubMed  Google Scholar 

  • Pinheiro F, Barros F, Palma-Silva C, Fay MF, Lexer C, Cozzolino S (2011) Phylogeography and genetic differentiation along the distributional range of the orchid Epidendrum fulgens: a Neotropical coastal species not restricted to glacial refugia. J Biogeogr 38:1923–1935

    Article  Google Scholar 

  • Pinheiro F, Cozzolino S, Barros F, Gouveia TM, Suzuki RM, Fay MF, Palma-Silva C (2013) Phylogeographic structure and outbreeding depression reveal early stages of reproductive isolation in the Neotropical orchid Epidendrum denticulatum. Evolution 67:2024–2039

    Article  PubMed  Google Scholar 

  • Ramirez J, Jarvis A (2008) High resolution statistically downscaled future climate surfaces. International Centre for Tropical Agriculture, CIAT. http://gisweb.ciat.cgiar.org/GCMPage

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schenk CJ, Viger RJ, Anderson CP (1999) Maps showing geology, oil and gas fields, and geologic provinces of South America. 97-470D. US Geological Survey, Denver Colorado. http://pubs.usgs.gov/of/1997/ofr-97-470/OF97-470D/

  • Schoener TW (1968) Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726

    Article  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 

  • Scopece G, Lexer C, Widmer A, Cozzolino S (2010) Polymorphism of postmating reproductive isolation within plant species. Taxon 59:1367–1374

    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 

  • Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng CF, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348

    Article  PubMed  Google Scholar 

  • Soltis DE, Buggs RJ, Doyle JJ, Soltis PS (2010) What we still don’t know about polyploidy. Taxon 59:1387–1403

    Google Scholar 

  • Ståhlberg D, Hedrén M (2009) Habitat differentiation, hybridization and gene flow patterns in mixed populations of diploid and autotetraploid Dactylorhiza maculata s.l. (Orchidaceae). Evol Ecol 23:295–328

    Article  Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Addison-Wesley, London

    Google Scholar 

  • Strasburg JL, Rieseberg LH (2008) Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris—large effective population sizes and rates of long-term gene flow. Evolution 62:1936–1950

    Article  PubMed Central  PubMed  Google Scholar 

  • Surget-Groba Y, Kay KM (2013) Restricted gene flow within and between rapidly diverging Neotropical plant species. Mol Ecol 22:4931–4942

    Article  PubMed  Google Scholar 

  • Tanksley SD, Zamir D, Rick CM (1981) Evidence for extensive overlap of sporophytic and gametophytic gene expression in Lycopersicon esculentum. Science 213:453–455

    Article  CAS  PubMed  Google Scholar 

  • Twyford AD, Kidner CA, Ennos RA (2014) Genetic differentiation and species cohesion in two widespread Central American Begonia species. Heredity 112:382–390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vega Y, Marques I, Castro S, Loureiro J (2013) Outcomes of extensive hybridization and introgression in Epidendrum (Orchidaceae): can we rely on species boundaries? PLoS One 8:e80662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zitari A, Scopece G, Helal NA, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank A. Ferreira and R.C. Marques for help during fieldwork. Funding for this study was provided by grants from FAPESP to FP (2009/15052-0), LRSG (2010/16353-1) and APM (2011/22215-3 and 2012/22077-2), and a PNPD/CAPES fellowship to F. P.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fábio Pinheiro.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pinheiro, F., Cardoso-Gustavson, P., Suzuki, R.M. et al. Strong postzygotic isolation prevents introgression between two hybridizing Neotropical orchids, Epidendrum denticulatum and E. fulgens . Evol Ecol 29, 229–248 (2015). https://doi.org/10.1007/s10682-015-9753-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-015-9753-z

Keywords

Navigation