Stamen construction, development and evolution in Salvia s.l.

Abstract

Lever-like stamens are among the most important floral traits in Salvia s.l. Their morphology, function and diversity were repeatedly studied to understand the lever mechanism and to reconstruct stamen evolution. The present paper reviews current knowledge on stamen diversity in Salvia species and combines morphogenetic and phylogenetic data. Five stamen types are distinguished based on absence vs. presence of versatile anthers, bithecate vs. monothecate anthers, curved vs. straight connective growth and presence vs. absence of the lower lever arm. Type I (no versatile anthers) is restricted to the four species of the Californian sect. Echinosphace. Versatile anthers evolved at least five times: Type II (bithectae) is the most common one in all old world Salvia s.l. clades, but also appears twice in America. Type III (monothectae, curved connective) is derived from type II (ontogenetic abbreviation). It is not restricted to the Eurasian-African clade I (Salvia s. str.) and the E-Asian clade IV-A, but also underlies some bee-pollinated American species. The new function of the lower lever arm to serve as a sterile barrier goes along with novel growth centres (ontogenetic addition). Type IV (monothecate, straight connective) characterises the majority of the American species (subgen. Calosphace). Type V (no lower lever arm) is derived by ontogenetic abbreviation and most likely homoplastic. It evolved at least four times independently, i.e. twice in Salvia s. str., once in the Californian clade II-B (sect. Audibertia) and once or several times in the East Asian clade. The study shows that stamen diversity results from few developmental changes. The latter appear in different combinations and support subclades rather than clades.

Keywords

• Inhibition,flower force,novel growth centers,ontogenetic abbreviation,ontogenetic addition,parallel evolution,phylogeny,staminal lever mechanism

Kaynakça

1. Baikova, E. (2002). Two ways of stamen development in the subgenus Calosphace (Salvia, Lamiaceae). Botanicheskii- Zhurnal 87, 71-78 (in Russian).Claßen-Bockhoff, R., & Speck, T. (2000). Diversity and evolution in Salvia - presentation of a new research project. Vitex 1, 3-4.
2. Claßen-Bockhoff, R., Crone, M., & Baikova, E. (2004a). Stamen development in Salvia L.: Homology reinvestigated. International Journal of Plant Science 165, 475-498.
3. Claßen-Bockhoff, R., Speck, T., Tweraser, E., Wester, P., Thimm, S., & Reith, M. (2004b). The staminal lever mechanism in Salvia L. (Lamiaceae): a key innovation for adaptive radiation? Organisms, Diversity & Evolution 4, 189-205.
4. Claßen-Bockhoff, R., Wester, P., & Tweraser, E. (2003). The staminal lever mechanism in Salvia L. (Lamiaceae) - a review. Plant Biology 5, 33-41.
5. Córdoba, S. A. & Cocucci, A. A. (2011). Flower power: its association with bee power and floral functional morphology in papilionate legumes. Annals of Botany 108, 919-931.
6. Correns, C. (1891). Zur Biologie und Anatomie der Salvienblüthe. Pringsheims Jahrbücher der Wissenschaftlichen Botanik 22, 190-240.
7. Drew, B.T., González-Gallegos, J.G., Xiang, C.L., Kriebel, R., Drummond, C.P., Walker, J.B., & Sytsma, K.J. (2017). Salvia united: The greatest good for the greatest number. Taxon 66, 133-145.
8. Drew, B. T., & Sytsma, K. J. (2012). Phylogenetics, biogeography, and staminal evolution in the tribe Mentheae (Lamiaceae). American Journal of Botany 99, 933-953.

9. Fragoso-Martínez, I., Martínez-Gordillo, M., Salazar, G.A., Sazatornil, F., Jenks, A. A., García Peña, M. de R., Barrera- Aveleida, G., Benitez-Vieyra, S., Magallón, S., Cornejo-Tenorio, G., & Granados Mendoza, C. (2017). Plant Systematics and Evolutio. doi.org/10.1007/s00606-017-1445-4
10. Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: Belknap Press.
11. Grant, V. (1994). Modes and origin of mechanical and ethological isolation in angiosperms. Proceedings of the NationalAcademy of Sciences 91, 3–10.
12. Harder, L. D., Jordan, C. Y., Gross, W. E., & Routley, M. B. (2004). Beyond floricentrism: The pollination function ofinflorescences. Plant Species Biology 19, 137-148.
13. Hedge, I. C. (1974). A revision of Salvia in Africa including Madagascar and the Canary Islands. Notes of the Royal BotanicGarden Edinburgh 33, 1-121.
14. Himmelbaur, W., & Stibal, E. (1933). Entwicklungsrichtungen in der Blütenregion der Gattung Salvia L. II.Staubgefäßtypen in der Gattung Salvia. Biologia generalis 8, 129-150.
15. Hrubý, K. (1934). Zytologie und Anatomie der mitteleuropäischen Salbei-Arten. Beihefte des Botanischen Centralblattes52, 298-380.
16. Müller, H. (1873). Die Befruchtung der Blumen durch Insekten und die gegenseitige Anpassung beider. Leipzig:Engelmann.
17. Naghiloo, S., Khodaverdi, M., Esmaillou, Z., Dadpour, & M. R., Rudall, P. (2014). Comparative floral development in the tribe Mentheae (Nepetoideae: Lamiaceae) and its bearing on the evolution of floral patterns in asteroids. Journal of Systematics and Evolution 52, 195–214.
18. Ott, D., Hühn, P., & Claßen-Bockhoff, R. (2016). Salvia apiana - A carpenter bee flower? Flora 221, 82–91.
19. Reith, M., Baumann, G., Claßen-Bockhoff, R., & Speck, T. (2007). New insights into the functional morphology of thelever mechanism of Salvia pratensis (Lamiaceae). Annals of Botany 100, 393-400.
20. Reith, M., Claßen-Bockhoff, R. & Speck,T. (2006). Biomechanics of Salvia flowers: The role of lever and flower tube in specialization on pollinators. In A. Herrel, T. Speck, N. P. Rowe (Eds.), Ecology and biomechanics - A mechanical approach to the ecology of animals and plants (123–145). Boca Raton: Taylor & Francis.
21. Reith M, Zona S. 2016. Nocturnal flowering and pollination of a rare Caribbean sage, Salvia arborescens (Lamiaceae). Neotropical Biodiversity 2: 115-123
22. Speck, T., Rowe, N., Civeyrel, L., Claßen-Bockhoff, R., Neinhuis, C., & Spatz, H. C. (2003). The potential of plant biomechanics in functional biology and systematics. In T. F. Stuessy, V. Mayer, & E. Hörandl (Eds.), Deep morphology. Toward a renaissance of morphology in plant systematics (241 – 271). Liechtenstein: Gantner.Sprengel, C. K. (1793). Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen. Berlin: Vieweg.
23. Stöbbe, J., Schramme, J., & Claßen-Bockhoff, R. (2016). Training experiments with Bombus terrestris and Apis mellifera on artificial ‘Salvia’ flowers. Flora 221, 92-99.
24. Thimm, S. (2008). Pollen-placement and pollen-portioning in diverse Salvia-species. Ph. D. Thesis, Mainz University, Germany.
25. Trapp, A. (1956a). Zur Morphologie und Entwicklungsgeschichte der Staubblätter sympetaler Blüten. Botanische Studien 5.
26. Trapp, A. (1956b). Entwicklungsgeschichtliche Untersuchungen über die Antherengestaltung sympetaler Blüten. Beiträge zur Biologie der Pflanzen 32, 279-312.
27. Troll, W. (1929). Roscoea purpurea Sm., eine Zingiberacee mit Hebelmechanismus in den Blüten. Mit Bemerkungen über die Entfaltung der fertilen Staubblätter von Salvia. Planta 7, 1-28.
28. Walker, J. B., & Sytsma, K. L., (2007). Staminal evolution in the genus Salvia (Lamiaceae): Molecular phylogenetic evidence for multiple origins of the staminal lever. Annals of Botany 100, 375-391.
29. Walker, J. B., Drew, B. T., & Sytsma, K. J. (2015). Unravelling species relationships and diversification within the iconic California floristic province sages (Salvia subgenus Audibertia, Lamiaceae). Systematic Botany 40, 826-844.
30. Walker, J. B., Sytsma, K. J., Treutlein, J., & Wink, M. (2004). Salvia (Lamiaceae) is not monophyletic: implications for the systematics, radiation, and ecological specializations of Salvia and tribe Mentheae. American Journal Botany 91, 1115- 1125.
31. Wester, P., & Claßen-Bockhoff, R. (2007). Floral diversity and pollen transfer mechanism in bird-pollinated Salvia species. Annals of Botany 100, 4101-421.
32. Wester, P., & Claßen-Bockhoff, R. (2011). Pollination syndromes of new world Salvia species with special reference to bird pollination. Annals of the Missouri Botanical Garden 98, 101-155.
33. Wester, P., Czarny, S., & Claßen-Bockhoff, R. (2012). The maintenance of nototriby by resupination -experimental studies in Salvia gravida Epling. 20. International Symposium `Biodiversity and Evolutionary Biology ́, 16 -19 September 2012 Mainz, Germany.
34. Westerkamp, C., & Claßen-Bockhoff, R. (2007). Bilabiate flowers: The ultimate response to bees? Annals of Botany 100, 361-374.
35. Will, M., & Claßen-Bockhoff, R. (2014). Why Africa matters: evolution of Old World Salvia (Lamiaceae) in Africa. Annals of Botany, 114: 61-83.
36. Will, M., & Claßen-Bockhoff, R. (2017). Time to split Salvia s.l. (Lamiaceae) - new insights from Old World Salvia phylogeny. Molecular Phylogenetics and Evolution 109, 33-58.
37. Will, M., Schmalz, N., & Claßen-Bockhoff, R. (2015). Towards a new classification of Salvia s.l.: (re)establishing the genus Pleudia Raf. Turkish Journal Botany 39, 693-707.
38. Zalewska, Z. (1928). Recherches sur l’évoltion des étamines, considérée du point de vue de leur adaptation à la pollinisation des fleurs de la Sauge (Salvia). Bulletin International de l’Academie Polonaise des Sciences et des Lettres 3, 133-160.