Phylogeny determines flower size-dependent sex allocation at flowering in a hermaphroditic family
Corresponding Author
A. L. Teixido
Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Madrid, Móstoles, Spain
Correspondence
A. L. Teixido, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-901 Belo Horizonte, Minas Gerais, Brazil
E-mail: [email protected]
Search for more papers by this authorV.G. Staggemeier
Department of Botany, São Paulo State University (UNESP), Institute of Biosciences, Phenology Lab, Rio Claro, São Paulo, Brazil
Search for more papers by this authorF. Valladares
Museo Nacional de Ciencias Naturales, MNCN-CSIC, Madrid, Spain
Search for more papers by this authorCorresponding Author
A. L. Teixido
Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Madrid, Móstoles, Spain
Correspondence
A. L. Teixido, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-901 Belo Horizonte, Minas Gerais, Brazil
E-mail: [email protected]
Search for more papers by this authorV.G. Staggemeier
Department of Botany, São Paulo State University (UNESP), Institute of Biosciences, Phenology Lab, Rio Claro, São Paulo, Brazil
Search for more papers by this authorF. Valladares
Museo Nacional de Ciencias Naturales, MNCN-CSIC, Madrid, Spain
Search for more papers by this authorAbstract
- In animal-pollinated hermaphroditic plants, optimal floral allocation determines relative investment into sexes, which is ultimately dependent on flower size. Larger flowers disproportionally increase maleness whereas smaller and less rewarding flowers favour female function. Although floral traits are considered strongly conserved, phylogenetic relationships in the interspecific patterns of resource allocation to floral sex remain overlooked. We investigated these patterns in Cistaceae, a hermaphroditic family.
- We reconstructed phylogenetic relationships among Cistaceae species and quantified phylogenetic signal for flower size, dry mass and nutrient allocation to floral structures in 23 Mediterranean species using Blomberg's K-statistic. Lastly, phylogenetically-controlled correlational and regression analyses were applied to examine flower size-based allometry in resource allocation to floral structures.
- Sepals received the highest dry mass allocation, followed by petals, whereas sexual structures increased nutrient allocation. Flower size and resource allocation to floral structures, except for carpels, showed a strong phylogenetic signal. Larger-flowered species allometrically allocated more resources to maleness, by increasing allocation to corollas and stamens.
- Our results suggest a major role of phylogeny in determining interspecific changes in flower size and subsequent floral sex allocation. This implies that flower size balances the male–female function over the evolutionary history of Cistaceae. While allometric resource investment in maleness is inherited across species diversification, allocation to the female function seems a labile trait that varies among closely related species that have diversified into different ecological niches.
Supporting Information
Filename | Description |
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plb12604-sup-0001-Supinfo.docWord document, 1.5 MB | Table S1. Growth form, location, climate data and mean flower size (diameter: cm ± SD; area: cm2 ± SD; N = 15 for all species) of the 23 species of Cistaceae used in the study. Compatibility systems for some species are also shown from the literature. Climate column also shows annual mean rainfall (mm) and annual mean temperature (°C) (Ninyerola et al. 2005, N = 20 years). Life form follows Arrington & Kubitzki (2003). Table S2. Mean ± SD (%) resource allocation to floral structures in the 23 studied species of Cistaceae in terms of dry mass, N and P. Concentrations are given in mmol g−1 dry mass. Total sample number for nutrient analyses (i.e. 1, 2, 3, 4 or 5 tubes used in digestions with sulphuric acid). Table S3. Details of fossil and secondary calibration points used in the Bayesian phylogenetic analysis of Cistaceae divergence. Table S4. GenBank accession number of rcbL gene and trnL-trnF spacer sequences and voucher for 45 Cistaceae species plus Hopea hainensis and Monotes madagascariensis (Dipterocarpaceae) as outgroup. Table S5. Pearson correlation coefficients between PIC values of the percentage resource allocation to floral structures in terms of dry mass, N and P in Cistaceae (N = 22 nodes in all cases). Figure S1. Flowers and individuals of the largest-flowered (A – Cistus ladanifer) and one of the smallest-flowered (B - Tuberaria guttata) species used in this study. Some individuals of these species show dark-coloured spots on their flowers. A large bee fly (Bombylidae) visiting C. ladanifer flower (bottom left). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Ackerly D.D. (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proceedings of the Natural Academy of Sciences USA, 106, 19699–19706.
- Aragón C.F., Méndez M., Escudero A. (2009) Survival costs of reproduction in a short-lived perennial plant: live hard, die young. American Journal of Botany, 96, 904–911.
- Armbruster W.S., Di Stilio V.S., Tuxill J.D., Flores T.C., Velásquez Runk J.L. (1999) Covariance and decoupling of floral and vegetative traits in nine Neotropical plants: a re-evaluation of Berg's correlation-pleiades concept. American Journal of Botany, 86, 39–55.
- Arrington J.M., Kubitzki K. (2003) Cistaceae. In: K. Kubitzki (Ed), The families and genera of vascular plants. Springer, Berlin, Germany, pp 62–70.
10.1007/978-3-662-07255-4_15 Google Scholar
- Ashman T.-L., Baker I. (1992) Variation in floral sex allocation with time of season and currency. Ecology, 73, 1237–1243.
- Barrio M., Teixido A.L. (2015) Sex-dependent selection on flower size in a large-flowered Mediterranean species: an experimental approach with Cistus ladanifer. Plant Systematics and Evolution, 301, 113–124.
- Bell G. (1985) On the function of flowers. Proceedings of the Royal Society of London series B, 224, 223–265.
- Bell C.D., Soltis D.E., Soltis P.S. (2010) The age and diversification of the angiosperms re-revisited. American Journal of Botany, 97, 1296–1303.
- Blomberg S.P., Garland T. (2002) Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology, 15, 899–910.
- Blomberg S.P., Garland T. Jr, Ives A.R. (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717–745.
- Bosch J. (1992) Floral biology and pollinators of three co-occurring Cistus species (Cistaceae). Botanical Journal of the Linnean Society, 109, 39–55.
- Brock M.T., Weinig C. (2007) Plasticity and environment-specific covariances: an investigation of floral-vegetative and within flower correlations. Evolution, 61, 2913–2924.
- Campbell D.R. (2000) Experimental tests of sex-allocation theory in plants. Trends in Ecology & Evolution, 15, 227–232.
- Campbell D.R., Weller S.G., Sakai A.K., Culley T.M., Dang P.N., Dunbar-Wallis A.K. (2011) Genetic variation and covariation in floral allocation of two species of Schiedea with contrasting levels of sexual dimorphism. Evolution, 65, 757–770.
- Carrió E., Güemes J. (2013) The role of a mixed mating system in the reproduction of a Mediterranean subshrub (Fumana hispidula, Cistaceae). Journal of Plant Research, 126, 33–40.
- Case A.L., Ashman T.-L. (2005) Sex-specific physiology and its implications for the costs of reproduction. In: E. G. Reekie, F. A. Bazzaz (Eds), Reproductive allocation in plants. Elsevier/Academic Press, Oxford, UK, pp 129–157.
- Chapin F.S. III, Vitousek P.M., Van Cleve K. (1986) The nature of nutrient limitation in plant communities. The American Naturalist, 127, 48–58.
- Charlesworth D., Charlesworth B. (1981) Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society, 15, 57–74.
- Charnov E.L. (1982) The theory of sex allocation. Princeton University Press, Princeton, NJ, USA.
- Charnov E.L., Bull J.J. (1986) Sex allocation, pollinator attraction and fruit dispersal in cosexual plantas. Journal of Theoretical Biology, 118, 321–325.
- Civeyrel L., Leclercq J., Demoly J.-P., Agnan Y., Quèbre N., Péllisier C., Otto T. (2011) Molecular systematics, character evolution, and pollen morphology of Cistus and Halimium. Plant Systematics and Evolution, 295, 23–54.
- Cruden R.B., Lyon D.L. (1985) Patterns of biomass allocation to male and female functions in plants with different mating systems. Oecologia, 66, 299–306.
- Dawson T.E., Geber M.A. (1999) Sexual dimorphism in physiology and morphology. In: M. A. Geber, T. E. Dawson, L. F. Delph (Eds), Gender and sexual dimorphism in flowering plants. Springer, Berlin, Germany, pp 175–215.
10.1007/978-3-662-03908-3_7 Google Scholar
- Dodd M.E., Silvertown J., Chase M.K. (1999) Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution, 53, 732–744.
- Drummond A.J., Suchard M.A., Xie D., Rambaut A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.
- Felsenstein J. (1985) Phylogenies and the comparative method. The American Naturalist, 125, 1–15.
- Forest F. (2009) Calibrating the tree of life: fossils, molecules and evolutionary timescales. Annals of Botany, 104, 789–794.
- Galen C. (2005) It never rains but then it pours: the diverse effects of water on flower integrity and function. In: E. Reekie, F. A. Bazzaz (Eds), Reproductive allocation in plants. Elsevier/Academic Press, Oxford, UK, pp 77–95.
10.1016/B978-012088386-8/50003-X Google Scholar
- Gómez J.M., Perfectti F., Lorite J. (2015) The role of pollinators in floral diversification in a clade of generalist flowers. Evolution, 69, 863–878.
- Goodwillie C., Sargent R.D., Eckert C.G., Elle E., Geber M.A., Johnston M.O., Kalisz S., Moeller D.A., Ree R.H., Vallejo-Marín M., Winn A.A. (2010) Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phytologist, 185, 311–321.
- Green A.J. (1999) Allometry of genitalia in insects and spiders: one size does not fit at all. Evolution, 53, 1621–1624.
- Guo H., Mazer S.J., Du G. (2010) Geographic variation in primary sex allocation per flower within and among 12 species of Pedicularis (Orobanchaceae): proportional male investment increases with elevation. American Journal of Botany, 97, 1334–1341.
- Guzmán B., Vargas P. (2005) Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnL-trnF, and matK sequences. Molecular Phylogenetics and Evolution, 37, 644–660.
- Guzmán B., Vargas P. (2009a) Historical biogeography and character evolution of Cistaceae (Malvales) based on analyses of plastid rbcL and trnL-trnF sequences. Organism Diversity and Evolution, 9, 83–99.
- Guzmán B., Vargas P. (2009b) Long-distance colonization of the Western Mediterranean by Cistus ladanifer (Cistaceae) despite the absence of special dispersal mechanisms. Journal of Biogeography, 36, 954–968.
- Herrera J. (1992) Flower variation and breeding systems in the Cistaceae. Plant Systematics and Evolution, 179, 245–255.
- de Jong T., Klinkhamer P. (2005) Evolutionary ecology of plant reproductive strategies. Cambridge University Press, Cambridge, UK.
- Kembel S.W., Cowan P.D., Helmus M.R., Cornwell W.K., Morlon H., Ackerly D.D., Blomberg S.P., Webb C.O. (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464.
- Kerkhoff A.J., Fagan W.F., Elser J.J., Enquist B.J. (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. The American Naturalist, 168, 103–122.
- Lloyd D.G. (1980) Sexual strategies in plants. I: an hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytologist, 86, 69–79.
- Lloyd D.G. (1992) Self- and cross-fertilization in plants. II. The selection of self-fertilization. International Journal of Plant Sciences, 153, 370–380.
- Lloyd D.G., Bawa K.S. (1984) Modification of the gender of seed plants in varying conditions. Evolutionary Biology, 17, 255–338.
- Méndez M., Traveset A. (2003) Sexual allocation in single-flowered hermaphroditic individuals in relation to plant and flower size. Oecologia, 137, 69–75.
- Miller M.A., Pfeiffer W., Schwartz T. (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Available from http://www.phylo.org (accessed 10 September 2014).
- Nandi O.I. (1998) Floral development and systematics of Cistaceae. Plant Systematics and Evolution, 212, 107–134.
- Oguro M., Sakai S. (2015) Relation between flower head traits and florivory in Asteraceae: a phylogenetically controlled approach. American Journal of Botany, 102, 407–416.
- Parachnowitsch A.L., Elle E. (2004) Variation in sex allocation and male–female trade-offs in six populations of Collinsia parviflora (Scrophulariaceae). American Journal of Botany, 91, 1200–1207.
- Rambaut A., Drummond A.J. (2007) Tracer version 1.4: MCMC trace analyses tool. Available from http://tree.bio.ed.ac.uk/software/tracer (accessed September 2014).
- Rodríguez-Pérez J. (2005) Breeding system, flower visitors and seedling survival of two endangered species of Helianthemum (Cistaceae). Annals of Botany, 95, 1229–1236.
- Roulston T.H., Cane J.H., Buchman S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions or phylogeny? Ecological Monographs, 70, 617–643.
- Smith S.D., Ané C., Baum D.A. (2008) The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution, 62, 793–806.
- Summers H.M., Hartwick S.M., Raguso R.A. (2015) Geographic variation in floral allometry suggests repeated transitions between selfing and outcrossing in a mixed mating plant. American Journal of Botany, 102, 1–13.
- Talavera S., Bastida F., Ortiz P.L., Arista M. (2001) Pollinator attendance and reproductive success in Cistus libanotis L. (Cistaceae). International Journal of Plant Sciences, 162, 343–352.
- Tébar F.J., Gil L., Llorens L. (1997) Reproductive biology of Helianthemum apenninum (L.) Mill. and H. caput-felis Boiss. (Cistaceae) from Mallorca (Balearic Islands, Spain). Acta Botanica Malacitana, 22, 53–63.
- Tedder A., Carleial S., Golębiewska M., Kappel C., Shimizu K.K., Stift M. (2015) Evolution of the selfing syndrome in Arabis alpina (Brassicaceae). PLoS ONE, 10, e0126618.
- Teixido A.L., Valladares F. (2014) Disproportionate carbon and water maintenance costs of large corollas in hot Mediterranean ecosystems. Perspectives in Plant Ecology, Evolution and Systematics, 16, 83–92.
- Teixido A.L., Barrio M., Valladares F. (2016) Size matters: understanding the conflict faced by large flowers in Mediterranean environments. Botanical Review, 82, 204–228.
- Thompson J.D. (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford, UK.
10.1093/acprof:oso/9780198515340.001.0001 Google Scholar
- Thompson K., Parkinson J.A., Band S.R., Spencer R.E. (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytologist, 136, 679–689.
- Ushimaru A., Nakata K. (2001) Evolution of flower allometry and its significance for pollination success in the deceptive orchid Pogonia japonica. International Journal of Plant Sciences, 162, 1307–1311.
- Zhao Z.-G., Meng J.-L., Fan B.-L., Du G.-Z. (2008) Size-dependent sex allocation in Aconitum gymnandrum (Ranunculaceae): physiological basis and effects of maternal family and environment. Plant Biology, 10, 694–703.