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Comparing Variational Properties of Homologous Floral and Vegetative Characters in Dalechampia scandens: Testing the Berg Hypothesis

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Abstract

The Berg hypothesis posits that, in plants with specialized pollination systems, floral characters should evolve to become integrated with each other and decoupled from vegetative characters. We test this hypothesis by comparing serially homologous and morphologically similar characters in leaves and involucral bracts in the Neotropical vine Dalechampia scandens, which has a specialized pollination system based on resin-collecting bees. The involucral bracts serve a number of specialized floral functions, including signaling and protection, that may put them under stronger selection for precision than the less specialized leaves. The homology and morphological similarity of the leaves and bracts allow us to make a sharper test of Berg’s hypothesis than is possible in most other systems. We found support for the hypothesis in that the bracts had lower coefficients of variation than the leaves for comparable traits. Also in support of the hypothesis, we found essentially zero phenotypic correlations between bracts and leaves at the same time that we found moderate correlations between different leaves and between different bracts. In contradiction to the hypothesis, however, we did not find higher correlations among traits within bracts than within leaves, and we found no evidence of bracts being more developmentally stable than the leaves.

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References

  • Ackerly, D. D., & Donoghue, M. J. (1998). Leaf size, sapling allometry, and Corner’s rules: Phylogeny and correlated evolution in maples (Acer). American Naturalist, 152, 767–791.

    Article  CAS  PubMed  Google Scholar 

  • Andersson, S. (1997). Genetic constraints on phenotypic evolution in Nigella (Ranunculaceae). Biological Journal of the Linnean Society, 62, 519–532.

    Article  Google Scholar 

  • Armbruster, W. S. (1982). Seed production and dispersal in Dalechampia (Euphorbiaceae): Divergent patterns and ecological consequences. American Journal of Botany, 69, 1429–1440.

    Article  Google Scholar 

  • Armbruster, W. S. (1984). The role of resin in angiosperm pollination: Ecological and chemical considerations. American Journal of Botany, 71, 1149–1160.

    Article  Google Scholar 

  • Armbruster, W. S. (1985). Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution, 39, 733–752.

    Article  Google Scholar 

  • Armbruster, W. S. (1988). Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology, 69, 1746–1761.

    Article  Google Scholar 

  • Armbruster, W. S. (1991). Multilevel analyses of morphometric data from natural plant populations: Insights into ontogenetic, genetic, and selective correlations in Dalechampia scandens. Evolution, 45, 1229–1244.

    Article  Google Scholar 

  • Armbruster, W. S. (1996). Evolution of floral morphology and function: An integrative approach to adaptation, constraint, and compromise in Dalechampia (Euphorbiaceae). In D. G. Lloyd & S. C. H. Barrett (Eds.), Floral biology: Studies on floral evolution in animal-pollinated plants (pp. 241–272). New York: Chapman & Hall.

    Google Scholar 

  • Armbruster, W. S. (1997). Exaptations link evolution of plant-herbivore and plant-pollinator interactions: A phylogenetic inquiry. Ecology, 78, 1661–1672.

    Google Scholar 

  • Armbruster, W. S. (2002). Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. Journal of Evolutionary Biology, 15, 468–486.

    Article  Google Scholar 

  • Armbruster, W. S., Antonsen, L., & Pélabon, C. (2005). Phenotypic selection on Dalechampia blossoms: Honest signaling affects pollination success. Ecology, 86, 3323–3333.

    Article  Google Scholar 

  • Armbruster, W. S., Di Stilio, V. S., Tuxill, J. D., Flores, T. C., & Velásquez-Runke, J. L. (1999). Covariance and decouping 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.

    Article  Google Scholar 

  • Armbruster, W. S., Howard, J. J., Clausen, T. P., Debevec, E. M., Loquvam, J. C., Matsuki, M., Cerendolo, B., & Andel, F. (1997). Do biochemical exaptation link evolution of plant defence and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines. American Naturalist, 149, 461–484.

    Article  Google Scholar 

  • Armbruster, W. S., Pélabon, C., Hansen, T. F., & Mulder, C. P. H. (2004). Floral integration, modularity, and precision: Distinguishing complex adaptations from genetic constraints. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 23–49). New York: Oxford University press.

    Google Scholar 

  • Armbruster, W. S., & Schwaegerle, K. E. (1996). Causes of covariation of phenotypic traits among populations. Journal of Evolutionary Biology, 9, 261–276.

    Article  Google Scholar 

  • Berg, R. L. (1959). A general evolutionary principle underlying the origin of developmental homeostasis. American Naturalist, 93, 103–105.

    Article  Google Scholar 

  • Berg, R. L. (1960). The ecological significance of correlation pleiades. Evolution, 17, 171–180.

    Article  Google Scholar 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499–516.

    Article  Google Scholar 

  • Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155–171.

    PubMed  CAS  Google Scholar 

  • Cheverud, J. M. (1988). A comparision of genetic and phenotypic correlations. Evolution, 42, 958–968.

    Article  Google Scholar 

  • Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.

    Google Scholar 

  • Cheverud, J. M. (2001). The genetic architecture of pleiotropic relations and differential epistasis. In G. P. Wagner (Ed.), The character concept in evolutionary biology (pp. 411–433). San Diego: Academic press.

    Google Scholar 

  • Conner, J. K., & Sterling, A. (1996). Selection for independence of floral and vegetative traits: Evidence from correlation patterns in five species. Canadian Journal of Botany, 74, 642–644.

    Article  Google Scholar 

  • Conner, J. K., & Via, S. (1993). Patterns of phenotypic and genetic correlations among morphological and life-history traits in wild radish, Raphanus Raphanistrum. Evolution, 47, 704–711.

    Article  Google Scholar 

  • Diggle, P. K. (1992). Development and the evolution of plant reproductive characters. In R. Wyatt (Ed.), Ecology and evolution of plant reprodution: New approaches (pp. 326–355). New York: Chapman & Hall.

    Google Scholar 

  • Freeman, D. C., Graham, J. H., & Emlen, J. M. (1993). Developmental stability in plants: Symmetries, stress and epigenesis. Genetica, 89, 97–119.

    Article  Google Scholar 

  • Guitián, J., Medrano, M., Herrera, C. M., & Sánchez-Lafuente, A. M. (2003). Variation in structural gender in the hermaphrodite Helleborus foetidus (Ranunculaceae): Whithin- and among-population patterns. Plant Systematics and Evolution, 241, 139–151.

    Article  Google Scholar 

  • Hansen, T. F. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems, 69, 83–94.

    Article  PubMed  Google Scholar 

  • Hansen, T. F. (2006). The evolution of genetic architecture. Annual Review of Ecology, Evolution & Systematics, 37, 123–157.

    Article  Google Scholar 

  • Hansen, T. F., Armbruster, W. S., & Antonsen, L. (2000). Comparative analysis of character displacement and spatial adaptations as illustrated by the evolution of Dalechampia blossoms. American Naturalist, 156, S17–S34.

    Article  Google Scholar 

  • Hansen, T. F., Armbruster, W. S., Carlson, M. L., & Pélabon, C. (2003a). Evolvability and genetic constaint in Dalechampia blossoms: Genetic correlations and conditional evolvability. Journal of Experimental Zoology, 296B, 23–39.

    Article  Google Scholar 

  • Hansen, T. F., Carter, A. J. R., & Pélabon, C. (2006). On adaptive accuracy and precision in natural populations. American Naturalist, 168, 168–181.

    Article  PubMed  Google Scholar 

  • Hansen, T. F., Pélabon, C., Armbruster, W. S., & Carlson, M. L. (2003b). Evolvability and genetic constraint in Dalechampia blossoms: Components of variance and measures of evolvability. Journal of Evolutionary Biology, 16, 754–765.

    Article  PubMed  Google Scholar 

  • Herrera, C. M., Cerda, X., Garcia, M. B., Guitian, J., Medrano, M., Rey, P. J., & Sanchez-Lafuente, A. M. (2002). Floral integration, phenotypic covariance structure and pollinator variation in bumblebee-pollinated Helleborus foetidus. Journal of Evolutionary Biology, 15, 108–121.

    Article  Google Scholar 

  • Ishii, H. S., & Morinaga, S. I. (2005). Intra- and inter-plant level correlations among floral traits in Iris gracilipes. Evolutionary Ecology, 19, 435–448.

    Article  Google Scholar 

  • Juenger, T., Pérez-Pérez, J. M., Bernal, S., & Micol, J. L. (2005). Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: Evidence for modular genetic architecture. Evolution and Development, 7, 259–271.

    Article  PubMed  CAS  Google Scholar 

  • Klingenberg, C. P. (2005). Developmental constraints, modules, and evolvability. In B. Hallgrimsson & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 219–247). New York: Elsevier Academic Press.

    Google Scholar 

  • Lynch M., & Walsh, B. (1998). Genetics and analysis of quantitative characters. Sunderland, Mass.: Sinauer Assocs. Inc.

    Google Scholar 

  • Magwene, P. M. (2001). New tools for studying integration and modularity. Evolution, 55, 1734–1745.

    PubMed  CAS  Google Scholar 

  • Mazer, S. J., Paz, H., & Bell, M. D. (2004). Life history, floral development, and mating system in Clarkia xantiana (Onagraceae): Do floral and whole plant rates of development evolve independently? American Journal of Botany, 91, 2041–2050.

    Google Scholar 

  • Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago, IL: The University of Chicago press.

    Google Scholar 

  • Pélabon, C., Hansen, T. F., Carlson, M. L., & Armbruster, W. S. (2004). Variational and genetic properties of developmental stability in Dalechampia scandens. Evolution, 53, 504–514.

    Google Scholar 

  • Pélabon, C., Hansen, T. F., Carlson, M. L., & Armbruster, W. S. (2006). Patterns of asymmetry in the twining vine Dalechampia scandens (Euphorbiaceae): Ontogenetic and hiearchial perspectives. New Phytologist, 170, 65–74.

    Article  PubMed  Google Scholar 

  • Riedl, R. J. (1977). A systems-analytical approach to macro-evolutionary phenomena. Quarterly Review of Biology, 52, 351–370.

    Article  PubMed  CAS  Google Scholar 

  • Riedl, R. J. (1978). Order in living organisms: A systems analysis of evolution. New York: Wiley.

    Google Scholar 

  • Van Valen, L. (2005). The statistics of variation. In B. Hallgrimsson & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 29–48). New York: Elsevier Academic Press.

    Google Scholar 

  • Verdu, M., & Gleiser, G. (2006). Adaptive evolution of reproductive and vegetatitve traits driven by breeding system. New Phytologist, 169, 409–417.

    Article  PubMed  Google Scholar 

  • Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and evolution of evolvability. Evolution, 50, 967–976.

    Article  Google Scholar 

  • Waitt, D. E., & Levin, D. A. (1993). Phenotypic integration and plastic correlations in Phlox-drummondii (polemoniaceae). American Journal of Botany, 80, 1224–1233.

    Article  Google Scholar 

  • Waitt, D. E., & Levin, D. A. (1998). Genetic and phenotypic correlations in plants: A botanical test of Cheverud’s conjecture. Heredity, 80, 310–319.

    Article  Google Scholar 

  • Webster, G. L., & Webster, B. D. (1972). Morphology and relationships of Dalechampia scandens (Euphorbiaceae). American Journal of Botany, 59, 573–586.

    Article  Google Scholar 

  • Willis, J. H., Coyne, J. A., & Kirkpatrick, M. (1991). Can one predict the evolution of quantitative characters without genetics? Evolution, 45, 441–444.

    Article  Google Scholar 

  • Winn, A. A. (1996). The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutionary Biology, 9, 737–752.

    Article  Google Scholar 

  • Worley, A. C., & Barrett, S. C. H. (2000). Evolution of floral display in Eichhornia paniculata (Pontederiaceae): Direct and correlated responses to selection on flower size and number. Evolution, 54, 1533–1545.

    PubMed  CAS  Google Scholar 

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Acknowledgements

This study is dedicated to the memory of Grady L. Webster (1927–2005), whose pioneering work on the morphology of Dalechampia scandens (with Barbara D. Webster), and on the evolution of euphorbs in general, laid the foundations for this study. Our research was supported by NSF Grant DEB-0444157 to TFH and DEB-0444745 to WSA. M. L. Carlson made the drawings, and we thank L. Antonsen, L. Dalen and T. Berge for seed collection in the field, and G. Fyhn-Hanssen for assistance in the greenhouse. We thank the reviewers for helpful comments on the manuscript.

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Authors and Affiliations

  1. Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo, P.O. Box 1050, 0316, Oslo, Norway

    Thomas F. Hansen

  2. Department of Biological Science, Florida State University, Tallahassee, FL, 32306, USA

    Thomas F. Hansen

  3. Department of Biology, Population Biology Centre, NTNU, 7491, Trondheim, Norway

    Christophe Pélabon

  4. Department of Biology, NTNU, 7491, Trondheim, Norway

    W. Scott Armbruster

  5. School of Biological Sciences, King Henry Building University of Portsmouth, Portsmouth, PO1 2DY, UK

    W. Scott Armbruster

  6. Institute of Arctic Biology, University of Alaska, Fairbanks, AK, 99775, USA

    W. Scott Armbruster

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  1. Thomas F. Hansen
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Correspondence to Thomas F. Hansen.

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Hansen, T.F., Pélabon, C. & Armbruster, W.S. Comparing Variational Properties of Homologous Floral and Vegetative Characters in Dalechampia scandens: Testing the Berg Hypothesis. Evol. Biol. 34, 86–98 (2007). https://doi.org/10.1007/s11692-007-9006-3

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