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Evolution of the staminode in a representative sample of Scrophularia and its role as nectar safeguard in three widespread species

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Abstract

Approximately 30 % of the genera of Scrophulariaceae s.str. have a staminode, which is the remnant of a sterile stamen. However, there are no studies of the functionality or evolutionary pattern of staminodes in that family. This paper investigates three Scrophularia species with different staminode sizes to determine if the staminode safeguards nectar from dilution by rainwater and if it influences pollinator behavior. We also study staminode evolution and ancestral state reconstruction onto a phylogeny containing 71 species and subspecies with four different staminode developmental stages: tiny, large, enormous, and absent. The results showed that large staminodes did not hinder nectar collection or modify pollinator-visiting time but acted as a barrier to reduce rainwater entry. The latter reduced the dilution of nectar, which did not occur with tiny staminodes. The phylogenetic study revealed that the ancestral state in the genus corresponds with the presence of a large staminode vs. the tiny and enormous staminodes that are considered as derived. The complete disappearance of the staminode has occurred independently at least twice. Events occurred that increased or reduced the staminode size in one of the clades (Clade II), which includes species of sect. Caninae; most of these events occurred during the Pleistocene (0.6–2.7 Ma).

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References

  • Aizen MA (2003) Down-facing flowers, hummingbirds and rain. Taxon 52:675–680. doi:10.2307/3647342

    Article  Google Scholar 

  • Alves GR, Peruchi A, Agostini K (2010) Polinização em área urbana: o estudo de caso de Jacaranda mimosifolia D. Don (Bignoniaceae). Bioikos, Campinas 24:31–41

  • Attar F, Riahi M, Daemi F, Aghabeigi F (2011) Preliminary molecular phylogeny of Eurasian Scrophularia (Scrophulariaceae) based on DNA sequence data from trnS-trnG and ITS regions. Plant Biosyst 145:857–865. doi:10.1080/11263504.2011.590826

    Article  Google Scholar 

  • Bittencourt NS Jr, Semir J (2006) Floral biology and late-acting self-incompatibility in Jacaranda racemosa (Bignoniaceae). Aust J Bot 54:315–324. doi:10.1071/BT04221

    Article  Google Scholar 

  • Carlbom C (1969) Evolutionary relationships in the genus Scrophularia L. Hereditas 61:287–301. doi:10.1111/j.1601-5223.1969.tb01844.x

    Article  Google Scholar 

  • Corbet S (1990) Pollination and the weather. Isr J Bot 39:13–30. doi:10.1080/0021213X.1990.10677131

    Google Scholar 

  • Dafni A (1996) Autumnal and winter pollination adaptations under Mediterranean conditions. Bocconea 5:171–181

    Google Scholar 

  • De Vos OC (1983) Scrophularia nodosa, adapted to wasp pollination? Acta Bot Neerlandica 32:345

    Google Scholar 

  • Dieringer G, Cabrera L (2001) Pollination ecology of bristle staminodia in Penstemon digitalis (Scrophulariaceae) and Jacaranda acutifolia (Bignoniaceae). Biotam 12:31–36

    Google Scholar 

  • Dieringer G, Cabrera L (2002) The interaction between pollinator size and the bristle staminode of Penstemon digitalis (Scrophulariaceae). Am J Bot 89:991–997. doi:10.3732/ajb.89.6.991

    Article  PubMed  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S (2010) Geneious v5.1. http://www.geneious.com. Accessed 20 January 2015

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710. doi:10.1371/journal.pbio.0040088

    Article  CAS  Google Scholar 

  • Drummond AJ, Ho SYW, Rawlence N, Rambaut A (2007) A rough guide to BEAST 1.4. http://code.google.com/p/beast-mcmc/downloads/list. Accessed 20 January 2015

  • Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320

    CAS  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi:10.1186/1471-2148-7-214

    Article  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973. doi:10.1093/molbev/mss075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, Oxford

    Google Scholar 

  • Fulton W (1886) The inflorescence, floral structure and fertilisation of Scrophularia aquatica and S. nodosa. Bot J Scotl 16:379–389. doi:10.1080/03746608609468296

    Google Scholar 

  • Grant V (1994) Historical development of ornithophily in the western North American flora. Proc Natl Acad Sci U S A 91:10407–10411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guimarães E, di Stasi LC, Maimoni-Rodella RCS (2008) Pollination biology of Jacaranda oxyphylla with an emphasis on staminode function. Ann Bot 102:699–711. doi:10.1093/aob/mcn152

    Article  PubMed Central  PubMed  Google Scholar 

  • Guzmán B, Vargas P (2005) Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnL-trnF, and matK sequences. Mol Phylogenet Evol 37:644–660. doi:10.1016/j.ympev.2005.04.026

    Article  PubMed  Google Scholar 

  • Hawk JL, Tepedino VJ (2007) The effect of staminode remove on female reproductive success in an Wyoming population of the endangered blowout Penstemon, Penstemon haydenii (Scrophulariaceae). Madroño 54:22–26. doi:10.3120/0024-9637(2007)54[22:TEOSRO]2.0.CO;2

    Article  Google Scholar 

  • Huang S-Q, Takahashi Y, Dafni A (2002) Why does the flower stalk of Pulsatilla cernua (Ranunculaceae) bend during anthesis? Am J Bot 89:1599–1603. doi:10.3732/ajb.89.10.1599

    Article  PubMed  Google Scholar 

  • Kornhall P, Bremer B (2004) New circumscription of the tribe Limoselleae (Scrophulariaceae) that includes the taxa of the tribe Manuleeae. Bot J Linn Soc 146:453–467. doi:10.1111/j.1095-8339.2004.00341.x

    Article  Google Scholar 

  • Kornhall P, Heidari N, Bremer B (2001) Selagineae and Manuleeae, two tribes or one? Phylogenetic studies in the Scrophulariaceae. Plant Syst Evol 228:199–218. doi:10.1007/s006060170029

    Article  Google Scholar 

  • Lall SS, Mill RR (1978) Scrophularia L. In: Davis PH (ed) Flora of Turkey 6. Edinburgh University Press, Edinburgh, pp 603–647

    Google Scholar 

  • Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis v2.74. http://org/mesquite/download/download.html. Accessed 20 January 2015

  • Maués MM, Oliveira PE, Kanashiro M (2008) Pollination biology in Jacaranda copaia (Aubl.) D. Don. (Bignoniaceae) at the "Floresta Nacional do Tapajós", Central Amazon, Brazil. Rev Bras Bot 31:517–527. doi:10.1590/S0100-84042008000300015

    Article  Google Scholar 

  • Müller H (1883) The fertilization of flowers. Macmillan, London

    Google Scholar 

  • Navarro-Pérez ML, López J, Fernández-Mazuecos M, Rodríguez-Riaño T, Vargas P, Ortega-Olivencia A (2013) The role of birds and insects in pollination shifts of Scrophularia (Scrophulariaceae). Mol Phylog Evol 69:239–254. doi:10.1016/j.ympev.2013.05.027

    Article  Google Scholar 

  • Navarro-Pérez ML, Vargas P, Fernández-Mazuecos M, López J, Valtueña FJ, Ortega-Olivencia A (2015) Multiple windows of colonization to Macaronesia by the dispersal-unspecialized Scrophularia since the Late Miocene. Perspect Plant Ecol. doi:10.1016/j.ppees.2015.05.002

  • Nicholls EIE, Dorken ME (2012) Sex-ratio variation and the function of staminodes in Aralia nudicaulis. Botany 90:575–585. doi:10.1139/b2012-016

    Article  Google Scholar 

  • Ortega-Olivencia A (2009) Scrophularia L. In: Benedí C, Rico E, Güemes J, Herrero A (eds) Flora Iberica 13. Real Jardín Botánico, CSIC, Madrid, pp 97–134

  • Ortega-Olivencia A, Devesa JA (1993a) Revisión del género Scrophularia L. (Scrophulariaceae) en la Península Ibérica e Islas Baleares. Monografías del Jardín Botánico de Madrid, Ruizia 11:1–157. CSIC, Madrid

  • Ortega-Olivencia A, Devesa JA (1993b) Floral rewards in some Scrophularia species (Scrophulariaceae) from the Iberian Peninsula and the Balearic Islands. Pl Syst Evol 184:139–158. doi:10.1007/BF00937432

    Article  Google Scholar 

  • Ortega-Olivencia A, Rodríguez-Riaño T, Pérez-Bote JL, López J, Mayo C, Valtueña FJ, Navarro-Pérez M (2012) Insects, birds and lizards as pollinators of the largest-flowered Scrophularia of Europe and Macaronesia. Ann Bot 109:153–167. doi:10.1093/aob/mcr255

    Article  PubMed Central  PubMed  Google Scholar 

  • Oxelman B, Kornhall P, Olmstead RG, Bremer B (2005) Further disintegration of Scrophulariaceae. Taxon 54:411–425

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer ver. 1.5. http://beast.bio.ed.ac.uk/Tracer.In. Accessed 20 January 2015

  • Rodríguez-Riaño T, Ortega-Olivencia A, López J, Pérez-Bote JL, Navarro-Pérez ML (2014) Main sugar composition of floral nectar in three species groups of Scrophularia (Scrophulariaceae) with different principal pollinators. Plant Biol 16:1075–1086. doi:10.1111/plb

    PubMed  Google Scholar 

  • Ronse-Decraene LP, Smets E (2001) Staminodes: their morphological and evolutionary significance. Bot Rev 67:351–402. doi:10.1007/BF02858099

    Article  Google Scholar 

  • Schremmer F (1959) Die bestäuber der Blüten von Scrophularia canina L. und Beobachtungen über postflorale Nektarabsonderung. Österr Bot Z 106:187–193

    Article  Google Scholar 

  • Scheunert A, Heubl G (2011) Phylogenetic relationships among New World Scrophularia L. (Scrophulariaceae): new insights inferred from DNA sequence data. Plant Syst Evol 291:69–89. doi:10.1007/s00606-010-0369-z

    Article  Google Scholar 

  • Scheunert A, Heubl G (2014) Diversification of Scrophularia (Scrophulariaceae) in the Western Mediterranean and Macaronesia—phylogenetic relationships, reticulate evolution and biogeographic patterns. Mol Phylogenet Evol 70:296–313. doi:10.1016/j.ympev.2013.09.023

    Article  PubMed  Google Scholar 

  • Shaw RJ (1962) The biosystematics of Scrophularia in western north America. Aliso 5:147–178

    Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166. doi:10.3732/ajb.92.1.142

    Article  CAS  PubMed  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288. doi:10.3732/ajb.92.1.142

    Article  CAS  PubMed  Google Scholar 

  • Sprengel CK (1793) Das entdeckte Geheimniss der Natur in Bau und in der Befrüchtung der Blumen. Berlin

  • Stiefelhagen H (1910) Systematische und pflanzengeographische Studien zur Kenntnis der Gattung Scrophularia. Vorarbeiten zu einer Monographie. Bot Jahrb 44:406–496

    Google Scholar 

  • Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacer of nuclear ribosomal DNA. Theor Appl Genet 89:26–32. doi:10.1007/BF00226978

    Article  CAS  PubMed  Google Scholar 

  • Trelease W (1881) The fertilization of Scrophularia. Bull Torrey Bot Club 8:133–140

    Article  Google Scholar 

  • Valtueña FJ, Ortega-Olivencia A, Rodríguez-Riaño T, Pérez-Bote JL, Mayo C (2013) Behaviour of pollinator insects within inflorescence of Scrophularia species from Iberian Peninsula. Plant Biol 15:328–334. doi:10.1111/j.1438-8677.2012.00644.x

    Article  PubMed  Google Scholar 

  • Vieira MF, Meira MRSA, Queiroz LP, Neto JAAM (1992) Polinização e reprodução de Jacaranda caroba (Vell.) DC. Bignoniaceae em área de Cerrado do sudeste do Brasil. Annais do 8ª Congresso da Sociedade Botânica de São Paulo. São Paulo, pp 13–19

  • Walker-Larsen J, Harder LD (2000) The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention. Am J Bot 87:1367–1384. doi:10.2307/2656866

    Article  CAS  PubMed  Google Scholar 

  • Walker-Larsen J, Harder LD (2001) Vestigial organs as opportunities for functional innovation: the example of the Penstemon staminode. Evolution 55:477–487. doi:10.1554/0014-3820(2001)055[0477:VOAOFF]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  • Wolfe AD, Shannon LD, Randle CP (2002) A phylogenetic and biogeographic analysis of the Cheloneae (Scrophulariaceae) based on ITS and matK sequence data. Syst Bot 27:138–148. doi:10.1043/0363-6445-27.1.138

    Google Scholar 

  • Wydler H (1828) Essai monographique sur le genre Scrofularia. Mém Soc Phys Genève 4:121–170. doi:10.3931/e-rara-10375

    Google Scholar 

  • Yanagizawa YANP, Maimoni-Rodella RCS (2007) Floral visitors and reproductive strategies in five melittophilous species of Bignoniaceae in Southeastern Brazil. Braz Arch Biol Technol 50:1043–1050. doi:10.1590/S1516-89132007000700015

    Article  Google Scholar 

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Acknowledgments

This research was supported by the Spanish Ministry of Science and Innovation through Project CGL2011-24140, co-financed by European Regional Development Fund. Partial funding was obtained from the Economy, Trade, and Innovation Council of Extremadura (CCV004). A FPI fellowship (BES-2009-011957) by the Spanish Ministry of Science and Innovation to MLN-P is greatly appreciated. The herbaria (E, MA, MJG, MO, SALA, UNEX) gave permission for DNA extraction from some specimens, and M. Kintgen (Denver Bot. Gard.), A. Amini Rad (Iranian Res. Inst. Pl. Protection), and M. Sequeira kindly sent us Scrophularia samples. We thank C. Mayo and J. Núñez (University of Extremadura) for helping in the field. We appreciate two anonymous reviewers for their constructive comments and suggestions. The English text was corrected and improved by L. Zonia and F. Donnelly (Bioedit, England).

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This article does not contain any studies with human participants performed by any of the authors.

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This article does not contain any studies with animal manipulation in our experiments. The activities carried out only involved the observation of insect pollinators, never their collection.

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Correspondence to Ana Ortega-Olivencia.

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Communicated by: Beverley Glover

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Rodríguez-Riaño, T., Valtueña, F.J., López, J. et al. Evolution of the staminode in a representative sample of Scrophularia and its role as nectar safeguard in three widespread species. Sci Nat 102, 37 (2015). https://doi.org/10.1007/s00114-015-1284-5

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