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BREEDING SYSTEMS AND SEED SIZE IN A NEOTROPICAL FLORA: TESTING EVOLUTIONARY HYPOTHESES
Corresponding Author
Steven M. Vamosi
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4 Canada
E-mail: [email protected]Search for more papers by this authorSusan J. Mazer
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106 USA
Search for more papers by this authorFernando Cornejo
Centro de Investigación y Capacitación del Río de Los Amigos, Amazon Conservation Association, Jirón Cusco 499, Puerto Maldonado, Madre de Dios, Peru
Search for more papers by this authorCorresponding Author
Steven M. Vamosi
Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4 Canada
E-mail: [email protected]Search for more papers by this authorSusan J. Mazer
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106 USA
Search for more papers by this authorFernando Cornejo
Centro de Investigación y Capacitación del Río de Los Amigos, Amazon Conservation Association, Jirón Cusco 499, Puerto Maldonado, Madre de Dios, Peru
Search for more papers by this authorCorresponding Editor: R. J. Marquis.
Abstract
A well-known, but largely untested, prediction in plant reproductive ecology is that dioecious taxa should produce larger, more, higher-quality, or better-defended seeds than cosexual taxa. Using a data set composed of 972 species in 104 families, representing the flora of the Tambopata Wildlife Reserve (Madre de Dios, Peru), we evaluated the first component of this prediction, examining ecological and evolutionary relationships between breeding system and mean seed size with two kinds of tests. First, we conducted cross-species analyses to determine whether species with different breeding systems differed significantly with respect to mean individual seed size. Second, we used a hypothesized phylogeny to identify pairs of the most closely related taxa or clades within the Tambopata community that differed with respect to breeding system. Comparing pair members allowed us to determine whether evolutionary divergence in breeding system (between taxa with unisexual vs. cosexual individuals) was consistently associated with evolutionary change in seed size. In both analyses, we controlled for potentially confounding effects of growth form by examining these relationships within woody and nonwoody taxa. Cross-species analyses revealed that dioecious species produced larger seeds than cosexual species among woody species, shrubs, lianas (each growth form analyzed separately), and all species pooled, but not among trees. Phylogenetically independent contrasts upheld the significant association between breeding system and seed size among woody taxa, lianas, and all taxa pooled, but not among shrubs. We discuss the implications of our findings for evolutionary hypotheses regarding associations between dioecy and seed size.
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Literature Cited
- Ackerly, D., and M. J. Donoghue . 1998. Leaf size, sapling allometry, and Corner's rules: a phylogenetic study of correlated evolution in maples (Acer). American Naturalist 152: 767–791.
- Baker, H. G. 1972. Seed weight in relation to environmental conditions in California. Ecology 53: 997–1010.
- Baker, H. G., and P. A. Cox . 1984. Further thoughts on dioecism and islands. Annals of the Missouri Botanical Garden 71: 244–253.
- Barot, S., and J. Gignoux . 2004. How do sessile dioecious species cope with their males. Theoretical Population Biology 66: 163–173.
- Bawa, K. S. 1980. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15–39.
- Bawa, K. S., and P. A. Opler . 1975. Dioecism in tropical forest trees. Evolution 29: 167–179.
- Bullock, S. H. 1985. Breeding systems in the flora of a tropical deciduous forest in Mexico. Biotropica 17: 287–301.
- Carlquist, S. 1974. Island biology. Columbia University Press, New York, New York, USA.
10.5962/bhl.title.63768 Google Scholar
- Carpenter, R. J., J. Read, and T. Jaffré . 2003. Reproductive traits of tropical rain-forest trees in New Caledonia. Journal of Tropical Ecology 19: 351–365.
- Chang, S. M. 2006. Female compensation through the quantity and quality of progeny in a gynodioecious plant, Geranium maculatum (Geraniaceae). American Journal of Botany 93: 263–270.
- Charlesworth, B., and D. Charlesworth . 1978. A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975–997.
- Charnov, E., and J. Maynard Smith . 1976. Why be an hermaphrodite. Nature 263: 125–126.
- Croat, T. B. 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford, California, USA.
- DeWalt, S. J., S. A. Schnitzer, and J. S. Denslow . 2000. Density and diversity of lianas along a chronosequence in a central Panamanian lowland forest. Journal of Tropical Ecology 16: 1–19.
- Dorken, M. E., J. Friedman, and S. C. H. Barrett . 2002. The evolution and maintenance of monoecy and dioecy in Sagittaria latifolia (Alismataceae). Evolution 56: 31–41.
- Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1–15.
- Foster, S. A. 1985. On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis. Botanical Review 52: 260–299.
- Foster, S. A., and C. H. Janson . 1985. The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66: 773–780.
- Gates, B. 1982. Banisteriopsis, Diplopterys (Malpighiaceae). Flora Neotropica Monograph 30: 1–237.
- Givnish, T. J. 1980. Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. Evolution 34: 959–972.
- Gross, C. L. 2005. A comparison of the sexual systems in the trees from the Australian tropics with other tropical biomes—more monoecy but why. American Journal of Botany 92: 907–919.
- Gustafsson, C., and C. Persson . 2002. Phylogenetic relationships among species of the neotropical genus Randia (Rubiaceae, Gardenieae) inferred from molecular and morphological data. Taxon 51: 661–674.
- Hammond, D. S., and V. K. Brown . 1995. Seed size of woody plants in relation to disturbance, dispersal, soil type in wet neotropical forests. Ecology 76: 2544–2561.
- Harmon, L. J., and J. B. Losos . 2005. The effect of intraspecific sample size on type I and type II error rates in comparative studies. Evolution 59: 2705–2710.
- Harper, J. L., and J. White . 1974. The demography of plants. Annual Review of Ecology and Systematics 5: 419–463.
10.1146/annurev.es.05.110174.002223 Google Scholar
- Harvey, P. H., and M. D. Pagel . 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, UK.
10.1093/oso/9780198546412.001.0001 Google Scholar
- Heilbuth, J. C. 2000. Lower species richness in dioecious clades. American Naturalist 156: 221–241.
- Heilbuth, J. C., K. Ilves, and S. P. Otto . 2001. The consequences of dioecy on seed dispersal: modeling the seed-shadow handicap. Evolution 55: 880–888.
- Ibarra-Manríquez, G., and K. Oyama . 1992. Ecological correlates of reproductive traits of Mexican rain forest trees. American Journal of Botany 79: 383–394.
- Janzen, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2: 465–492.
10.1146/annurev.es.02.110171.002341 Google Scholar
- Jurado, E., M. Westoby, and D. Nelson . 1991. Diaspore weight, dispersal, growth form and perenniality of central Australian plants. Journal of Ecology 79: 811–830.
- J. W. Kadereit 2004. The families and genera of vascular plants. Volume VII. Flowering plants. Dicotyledons: Lamiales (except Acanthaceae including Avicenniaceae) Springer-Verlag, Berlin, Germany.
- J. W. Kadereit, and C. Jeffrey . 2007. The families and genera of vascular plants. Volume VII. Flowering plants. Eudicots: Asterales Springer-Verlag, Berlin, Germany.
- Kelly, C. K. 1995. Seed size in tropical trees: a comparative study of factors affecting seed size in Peruvian angiosperms. Oecologia 102: 377–388.
- Koelewijn, H. P., and J. M. M. Van Damme . 2005. Effects of seed size, inbreeding and maternal sex on offspring fitness in gynodioecious Plantago coronopus. Journal of Ecology 93: 373–383.
- Kress, W. J. 1986. The systematic distribution of vascular epiphytes: an update. Selbyana 9: 2–22.
- K. Kubitzki 1998a. The families and genera of vascular plants. Volume III. Flowering plants. Monocotyledons: Lilianae (except Orchidaceae) Springer-Verlag, Berlin, Germany.
- K. Kubitzki 1998b. The families and genera of vascular plants. Volume IV. Flowering plants. Monocotyledons: Alismatanae and Commelinanae Springer-Verlag, Berlin, Germany.
- K. Kubitzki 2004. The families and genera of vascular plants. Volume VI. Flowering plants. Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales Springer-Verlag, Berlin, Germany.
- K. Kubitzki 2007. The families and genera of vascular plants. Volume IX. Flowering plants. Eudicots: Berberidopsidales, Buxales, Crossomatales, Fabales p.p., Geraniales, Gunnerales, Myrtales p.p., Proteales, Saxifragales, Vitales, Zygophyllales, Clusiaceae Alliance, Passifloraceae Alliance, Dilleniaceae, Huaceae, Picramniaceae, Sabiaceae Springer-Verlag, Berlin, Germany.
- K. Kubitzki, and C. Bayer . 2003. The families and genera of vascular plants. Volume V. Flowering plants. Dicotyledons: Capp1rales, Malvales and Non-betalain Caryophyllales Springer-Verlag, Berlin, Germany.
- K. Kubitzki, J. G. Rohwer, and V. Bittrich . 1993. The families and genera of vascular plants. Volume II. Flowering plants. Dicotyledons: Magnoliid, Hamamelid and Caryophyllid families Springer-Verlag, Berlin, Germany.
- Laurance, W. F., H. E. M. Nascimento, S. G. Laurance, R. Condit, S. D'Angelo, and A. Andrade . 2004. Inferred longevity of Amazonian rainforest trees based on a long-term demographic study. Forest Ecology and Management 190: 131–143.
- Leishman, M. R., and M. Westoby . 1994. Hypotheses on seed size: tests using the semiarid flora of western New South Wales, Australia. American Naturalist 143: 890–906.
- Leishman, M. R., M. Westoby, and E. Jurado . 1995. Correlates of seed size variation: a comparison among five temperate floras. Journal of Ecology 83: 517–529.
- Lenza, E., and P. E. Oliveira . 2005. Biologia reprodutiva de Tapirira guianensis Aubl. (Anacardiaceae), uma espécie dióica em mata de galeria do Triângulo Mineiro, Brasil. Revista Brasileira de Botânica 28: 179–190.
10.1590/S0100-84042005000100015 Google Scholar
- Lloyd, D. G. 1980. The distributions of gender in four angiosperm species illustrating two evolutionary pathways to dioecy. Evolution 34: 123–134.
- Lord, J., J. Egan, T. Clifford, E. Jurado, M. Leishman, D. Williams, and M. Westoby . 1997. Larger seeds in tropical floras: consistent patterns independent of growth form and dispersal mode. Journal of Biogeography 24: 205–211.
- Matallana, G., T. Wendt, D. S. D. Araujo, and F. R. Scarano . 2005. High abundance of dioecious plants in a tropical coastal vegetation. American Journal of Botany 92: 1513–1519.
- Mazer, S. J. 1989. Ecological, taxonomic, and life history correlates of seed mass among Indiana Dune angiosperms. Ecological Monographs 59: 153–175.
- Mazer, S. J. 1990. Seed mass variation of Indiana Dune genera and families: taxonomic and ecological correlates. Evolutionary Ecology 4: 326–358.
- Mitchell, C. H., and P. K. Diggle . 2005. The evolution of unisexual flowers: morphological and functional convergence result from diverse developmental transitions. American Journal of Botany 92: 1068–1076.
- Moles, A. T., D. D. Ackerly, C. O. Webb, J. C. Tweddle, J. B. Dickie, A. J. Pitman, and M. Westoby . 2005a. Factors that shape seed mass evolution. Proceedings of the National Academy of Sciences (USA) 102: 10540–10544.
- Moles, A. T., D. D. Ackerly, C. O. Webb, J. C. Tweddle, J. B. Dickie, and M. Westoby . 2005b. A brief history of seed size. Science 307: 576–580.
- Moles, A. T., D. S. Falster, M. R. Leishman, and M. Westoby . 2004. Small-seeded species produce more seeds per square metre of canopy per year, but not per individual per lifetime. Journal of Ecology 92: 384–396.
- Moles, A. T., and M. Westoby . 2004. Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92: 372–383.
- Muenchow, G. E. 1987. Is dioecy associated with fleshy fruit. American Journal of Botany 74: 287–293.
- Negrelle, R. R. B. 2002. The Atlantic forest in the Volta Velha Reserve: a tropical rain forest site outside the tropics. Biodiversity and Conservation 11: 887–919.
- Osunkoya, O. O. 2003. Two-sex population projection of the endemic and dioecious rainforest shrub, Gardenia actinocarpa (Rubiaceae). Biological Conservation 114: 39–51.
- Pennington, T. D., C. Reynel, and A. Daza . 2004. Illustrated guide to the trees of Peru. David Hunt, Sherborne, UK.
- Prinzing, A., W. Durka, S. Klotz, and R. Brandl . 2001. The niche of higher plants: evidence for phylogenetic conservatism. Proceedings of the Royal Society B 268: 2383–2389.
- Putz, F. E. 1984. The natural history of lianas on Barro Colorado Island, Panama. Ecology 65: 1713–1724.
- Putz, F. E. 1990. Liana stem diameter growth and mortality rates on Barro Colorado Island, Panama. Biotropica 22: 103–105.
- Queenborough, S. A., D. F. R. P. Burslem, N. C. Garwood, and R. Valencia . 2007. Determinants of biased sex ratios and inter-sex costs of reproduction in dioecious tropical forest trees. American Journal of Botany 94: 67–78.
- Ramula, S., and P. Mutikainen . 2003. Sex allocation of females and hermaphrodites in the gynodioecious Geranium sylvaticum. Annals of Botany 92: 207–213.
- Renner, S. S., L. Beenken, G. W. Grimm, A. Kocyan, and R. E. Ricklefs . 2007. The evolution of dioecy, heterodichogamy, and labile sex expression in Acer. Evolution 61: 2701–2719.
- Renner, S. S., and R. E. Ricklefs . 1995. Dioecy and its correlates in the flowering plants. American Journal of Botany 82: 596–606.
- Renner, S. S., and H. Won . 2001. Repeated evolution of dioecy from monoecy in Siparunaceae (Laurales). Systematic Biology 50: 700–712.
- Sakai, A. K., W. L. Wagner, D. M. Ferguson, and D. R. Herbst . 1995a. Biogeographical and ecological correlates of dioecy in the Hawaiian flora. Ecology 76: 2530–2543.
- Sakai, A. K., W. L. Wagner, D. M. Ferguson, and D. R. Herbst . 1995b. Origins of dioecy in the Hawaiian flora. Ecology 76: 2517–2529.
- Seidler, T. G., and J. B. Plotkin . 2006. Seed dispersal and spatial pattern in tropical trees. PLoS Biology 4: e344.
- Shykoff, J. A., S. O. Kolokotronis, C. L. Collin, and M. Lopez-Villavicencio . 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1–9.
- Sleumer, H. O. 1984. Olacaceae. Flora Neotropica Monograph 38: 1–159.
- Stevens, P. F. 2004. Angiosperm Phylogeny Website. Version 5, May 2004 〈http://www.mobot.org/MOBOT/research/APweb/〉.
- Steyermark, J. A., P. E. Berry, and B. K. Holst . 1995. Flora of the Venezuelan Guyana. Volume 2. Pteridophytes. Spermatophytes (Acanthaceae–Araceae). Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, and B. K. Holst . 1997. Flora of the Venezuelan Guyana. Volume 3. Araliaceae–Cactaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, and B. K. Holst . 1998. Flora of the Venezuelan Guyana. Volume 4. Caesalpiniaceae–Ericaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, K. Yatskievych, and B. K. Holst . 1999. Flora of the Venezuelan Guyana. Volume 5. Eriocaulaceae–Lentibulariaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, K. Yatskievych, and B. K. Holst . 2001. Flora of the Venezuelan Guyana. Volume 6. Liliaceae–Myrsinaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, K. Yatskievych, and B. K. Holst . 2003. Flora of the Venezuelan Guyana. Volume 7. Myrtaceae–Plumbaginaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, K. Yatskievych, and B. K. Holst . 2004. Flora of the Venezuelan Guyana. Volume 8. Poaceae–Rubiaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Steyermark, J. A., P. E. Berry, K. Yatskievych, and B. K. Holst . 2005. Flora of the Venezuelan Guyana. Volume 9. Rutaceae–Zygophyllaceae. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
- Thomson, J. D., and S. C. H. Barrett . 1981. Selection for outcrossing, sexual selection and the evolution of dioecy in plants. American Naturalist 118: 443–449.
- Vamosi, J. C., T. M. Knight, J. Steets, S. J. Mazer, M. Burd, and T.-L. Ashman . 2006. Pollination decays in biodiversity hotspots. Proceedings of the National Academy of Sciences (USA) 103: 956–961.
- Vamosi, J. C., S. P. Otto, and S. C. H. Barrett . 2003. Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology 16: 1006–1018.
- Vamosi, J. C., and S. M. Vamosi . 2004. The role of diversification in causing the correlates of dioecy. Evolution 58: 723–731.
- Vamosi, J. C., S. M. Vamosi, and S. C. H. Barrett . 2006. Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae). Proceedings of the Royal Society B 273: 2401–2407.
- Vamosi, J. C., Y. Zhang, and W. G. Wilson . 2007. Animal dispersal dynamics promoting dioecy over hermaphroditism. American Naturalist 170: 485–491.
- Vamosi, S. M. 2006. A reconsideration of the reproductive biology of the Atlantic forest in the Volta Velha Reserve. Biodiversity and Conservation 15: 1417–1424.
- Vamosi, S. M., and J. C. Vamosi . 2005. Endless tests: guidelines for analysing non-nested sister-group comparisons. Evolutionary Ecology Research 7: 567–579.
- Watson, L., and M. J. Dallwitz . 1992. onwards. The families of flowering plants: descriptions, illustrations, identification, and information retrieval. Version: 1st June 2007 〈http://delta-intkey.com/angio/www/index.htm〉.
- Webb, C. J. 1979. Breeding systems and the evolution of dioecy in New Zealand apioid Umbelliferae. Evolution 33: 662–672.
- Webb, C. O., D. D. Ackerly, and S. W. Kembel . 2007. Phylocom: software for the analysis of community phylogenetic structure and character evolution, with phylogeny tools. Version 3.41 〈http://www.phylodiversity.net/phylocom/〉.
- Webb, C. O., and M. J. Donoghue . 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5: 181–183.
- Weckerle, C. S., and R. Rutishauser . 2005. Gynoecium, fruit and seed structure of Paullinieae (Sapindaceae). Botanical Journal of the Linnean Society 147: 159–189.
- Wilson, W. G., and L. D. Harder . 2003. Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy. American Naturalist 162: 220–241.
- Woodson, R. E. Jr., R. W. Schery, and T. B. Croat . 1976. Flora of Panama. Part VI. Family 108. Sapindaceae. Annals of the Missouri Botanical Garden 63: 419–540.
- Yampolsky, C., and H. Yampolsky . 1922. Distribution of sex forms in the phanerogamic flora. Bibliotheca Genetica 3: 1–62.
- Zhang, S. T., G. Z. Du, and J. K. Chen . 2004. Seed size in relation to phylogeny, growth form and longevity in a subalpine meadow on the east of the Tibetan Plateau. Folia Geobotanica 39: 129–142.
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