Evolutionary Ecology

, Volume 21, Issue 6, pp 765–782 | Cite as

Multivariate selection shapes environment-dependent variation in the clonal morphology of a red seaweed

  • Keyne MonroEmail author
  • Alistair G. B. Poore
  • Robert Brooks
Original Paper


Within-individual strategies of variation (e.g., phenotypic plasticity) are particularly relevant to modular organisms, in which ramets of the same genetic individual may encounter diverse environments imposing diverse patterns of selection. Hence, measuring selection in heterogeneous environments is essential to understanding whether environment-dependent phenotypic change enhances the fitness of modular individuals. In sublittoral marine habitats, competition for light and space among modular taxa generates extreme patchiness in resource availability. Little is known, however, of the potential for plasticity within individuals to arise from spatially-variable selection in such systems. We tested whether plasticity enhances genet-level fitness in Asparagopsis armata, a clonal seaweed in which correlated traits mediate morphological responses to variation in light. Using the capacity for rapid, clonal growth to measure fitness, we identified aspects of ramet morphology targeted by selection in two contrasting light environments and compared patterns of selection across environments. We found that directional selection on single traits, coupled with linear and nonlinear selection on multi-trait interactions, shape ramet morphology within environments and favor different phenotypes in each. Evidence of environment-dependent, multivariate selection on correlated traits is novel for any marine modular organism and demonstrates that seaweeds, such as A. armata, may potentially adapt to environmental heterogeneity via plasticity in clonal morphology.


Adaptation Canonical rotation Clonal morphology Correlated traits Modular organisms Multivariate selection Plasticity Seaweed 



This research was supported by an Australian Postgraduate Award to K. Monro and the Australian Research Council Discovery Project DP0208481 to A. Poore. We thank M. Head, K. Donohue and two anonymous reviewers for insightful comments on an earlier draft of this manuscript.


  1. Arenas F, Viejo RM, Fernandez C (2002) Density-dependent regulation in an invasive seaweed: responses at plant and modular levels. J Ecol 90:820–829CrossRefGoogle Scholar
  2. Arnold SJ, Pfrender ME, Jones AG (2001) The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112–113:9–32PubMedCrossRefGoogle Scholar
  3. Ballaré CL, Scopel AL, Sanchez RA (1997) Foraging for light: photosensory ecology and agricultural implications. Plant Cell Environ 20:820–825CrossRefGoogle Scholar
  4. Bisgaard S, Ankenman B (1996) Standard errors for the eigenvalues in second-order response surface models. Technometrics 38:238–246CrossRefGoogle Scholar
  5. Björklund M (2003) Variation and selection––what are we measuring? Acta Zoologica Fennica 40:387–394Google Scholar
  6. Blows MW, Brooks R (2003) Measuring non-linear selection. Am Nat 162:815–820PubMedCrossRefGoogle Scholar
  7. Blows MW, Brooks R, Kraft PG (2003) Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies. Evolution 57:1622–1630PubMedGoogle Scholar
  8. Blows MW, Hoffmann AA (2005) A reassessment of genetic limits to evolutionary change. Ecology 86:1371–1384CrossRefGoogle Scholar
  9. Bonin DR, Hawkes MW (1987) Systematics and life histories of New Zealand Bonnemaisoniaceae (Bonnemaisoniales, Rhodophyta): 1. The genus Asparagopsis. NZ J Bot 25:577–590Google Scholar
  10. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155CrossRefGoogle Scholar
  11. Brodie ED III, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10:313–318CrossRefGoogle Scholar
  12. Brooks R, Hunt J, Blows MW, Smith MJ, Bussière LF, Jennions MD (2005) Experimental evidence for multivariate stabilizing sexual selection. Evolution 59:871–880PubMedGoogle Scholar
  13. Chenoweth SF, Blows MW (2005) Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata. Am Nat 165:281–289PubMedCrossRefGoogle Scholar
  14. Collado-Vides L (2002a) Clonal architecture in marine macroalgae: ecological and evolutionary perspectives. Evol Ecol 15:531–545CrossRefGoogle Scholar
  15. Collado-Vides L (2002b) Morphological plasticity of Caulerpa prolifera in relation to growth form in a coral reef lagoon. Bot Mar 45:123–129CrossRefGoogle Scholar
  16. Collado-Vides L, Robledo D (1999) Morphology and photosynthesis of Caulerpa (Chlorophyta) in relation to growth form. J Phycol 35:325–330CrossRefGoogle Scholar
  17. Dayton PK (1975) Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol Monogr 45:137–159CrossRefGoogle Scholar
  18. de Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82PubMedCrossRefGoogle Scholar
  19. de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants ––the foraging concept reconsidered. Journal of Ecology 83:143–152CrossRefGoogle Scholar
  20. Dixon PS (1964) Asparagopsis in Europe. Nature 204:902CrossRefGoogle Scholar
  21. Dong M (1993) Morphological plasticity of the clonal herb Lamiastrum galeobdolon (L.) Ehrend. & Polatschek in response to partial shading. New Phytol 124:291–300CrossRefGoogle Scholar
  22. Donohue K, Messiqua D, Pyle EH, Heschel MS, Schmitt J (2000) Evidence of adaptive divergence in plasticity: Density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54:1956–1968PubMedGoogle Scholar
  23. Draper NR, John JA (1988) Response surface designs for quantitative and qualitative variables. Technometrics 30:423–428CrossRefGoogle Scholar
  24. Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465CrossRefGoogle Scholar
  25. Gardner SN, Mangel M (1997) Can a clonal organism escape senescence? Am Nat 150:462–490 CrossRefPubMedGoogle Scholar
  26. Gaylord B, Blanchette CA, Denny MW (1994) Mechanical consequences of size in wave-swept algae. Ecol Monogr 64:287–313CrossRefGoogle Scholar
  27. Green PJ, Silverman B W (1994) Nonparametric regression and generalized linear models: a roughness penalty approach. Chapman & Hall, New YorkGoogle Scholar
  28. Griffith TM, Sultan SE (2005) Shade tolerance plasticity in response to neutral vs green shade cues in Polygonum species of contrasting ecological breadth. New Phytol 166:141–148PubMedCrossRefGoogle Scholar
  29. Guiry MD, Dawes CJ (1992) Daylength, temperature and nutrient control of tetrasporogenesis in Asparagopsis armata (Rhodophyta). J Exp Mar Biol Ecol 158:197–217CrossRefGoogle Scholar
  30. Harper JL (1985) Modules, branches and the capture of resources. In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 1–34Google Scholar
  31. Henry HAL, Aarssen LW (1997) On the relationship between shade tolerance and shade avoidance strategies in woodland plants. Oikos 80:575–582CrossRefGoogle Scholar
  32. Hood GM (2004) Poptools 2.6. Available at
  33. Huber H, Hutchings MJ (1997) Differential response to shading in orthotropic and plagiotropic shoots of the clonal herb Glechoma hirsuta. Oecologia 112:485–491CrossRefGoogle Scholar
  34. Huber H, Kane NC, Heschel MS, von Wettberg EJ, Banta J, Leuck A, Schmitt J (2004) Frequency and microenvironmental pattern of selection on plastic shade-avoidance traits in a natural population of Impatiens capensis. Am Nat 163:548–563PubMedCrossRefGoogle Scholar
  35. Huber H, Lukacs S, Watson M A (1999) Spatial structure of stoloniferous herbs: an interplay between structural blue-print, ontogeny and phenotypic plasticity. Plant Ecol 141:107–115CrossRefGoogle Scholar
  36. Huber H, Stuefer JF (1997) Shade-induced changes in the branching pattern of a stoloniferous herb: functional response or allometric effect? Oecologia 110:478–486CrossRefGoogle Scholar
  37. Huey RB, Carlson M, Crozier L, Frazier M, Hamilton H, Harley C, Hoang A, Kingsolver JG (2002) Plants versus animals: do they deal with stress in different ways? Integr Comp Biol 42:415–423CrossRefGoogle Scholar
  38. Hughes T P, Connell JH (1987) Population dynamics based on size or age? A reef-coral analysis. Am Nat 129:818–829CrossRefGoogle Scholar
  39. Jackson JBC, Coates AG (1986) Life cycles and the evolution of clonal (modular) animals. Philos Trans Roy Soc B 313:7–22CrossRefGoogle Scholar
  40. Jormalainen V, Honkanen T (2004) Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus. J Evol Biol 17:807–820PubMedCrossRefGoogle Scholar
  41. Kaandorp JA, Kübler J (2001) The algorithmic beauty of seaweeds, sponges and corals. Springer-Verlag, AmsterdamGoogle Scholar
  42. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261CrossRefPubMedGoogle Scholar
  43. Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, CambridgeGoogle Scholar
  44. Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33:402–416CrossRefGoogle Scholar
  45. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  46. Lasker HR (1990) Clonal propagation and population dynamics of a gorgonian coral. Ecology 71:1578–1589CrossRefGoogle Scholar
  47. Lasker HR, Coffroth MA (1999) Responses of clonal reef taxa to environmental change. Am Zool 39:92–103Google Scholar
  48. Lewontin RC (1978) Adaptation. Sci Am 239:157–169CrossRefGoogle Scholar
  49. Lovett Doust L (1981) Population dynamics and local specialization in a clonal perennial (Ranunculus repens). J Ecol 69:743–755CrossRefGoogle Scholar
  50. Lüning K (1981) Light. In: Lobban CS, Wynne MJ (eds) The biology of seaweeds. Blackwell, Oxford, pp 326–366Google Scholar
  51. Manly BFJ (2001) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall/C.R.C. Press, Boca RatonGoogle Scholar
  52. Middelboe AL, Binzer T (2004) Importance of canopy structure on photosynthesis in single- and multi-species assemblages of marine macroalgae. Oikos 107:422–432CrossRefGoogle Scholar
  53. Mitchell-Olds T, Shaw RG (1987) Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161CrossRefGoogle Scholar
  54. Monro K, Poore AGB (2005) Light quantity and quality induce shade-avoiding plasticity in a marine macroalga. J Evol Biol 18:426–35PubMedCrossRefGoogle Scholar
  55. Nishihara GN, Terada R, Noro T (2004) Photosynthesis and growth rates of Laurencia brongniartii J. Agardh (Rhodophyta, Ceramiales) in preparation for cultivation. J Appl Phycol 16:303–308CrossRefGoogle Scholar
  56. Nychka D (2004) Fields: tools for spatial data. R package version 1.5.
  57. Pan JJ, Price JS (2002) Fitness and evolution in clonal plants: the impact of clonal growth. Evol Ecol 15:583–600CrossRefGoogle Scholar
  58. Phillips PC, Arnold SJ (1989) Visualizing multivariate selection. Evolution 43:1209–1222CrossRefGoogle Scholar
  59. Pilson D 2000. The evolution of plant response to herbivory: Simultaneously considering resistance and tolerance in Brassica rapa. Evol Ecol 14:457–489CrossRefGoogle Scholar
  60. Preston KA, Ackerly DD (2004) The evolution of allometry in modular organisms. In: Pigliucci M, Preston KA (eds) Modularity and Phenotypic Complexity. Oxford University Press, Oxford, pp 80–106Google Scholar
  61. Pringle A, Chen D, Taylor JW (2003) Sexual fecundity is correlated to size in the lichenized fungus Xanthoparmelia cumberlandia. Bryologist 106:221–225CrossRefGoogle Scholar
  62. Puijalon S, Bornette G, Sagnes P (2005) Adaptations to increasing hydraulic stress: morphology, hydrodynamics and fitness of two higher aquatic plant species. J Exp Bot 56:777–786PubMedCrossRefGoogle Scholar
  63. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  64. R Development Core Team (2004) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  65. Rasband WS (2005) ImageJ 1.34. U. S. National Institutes of Health, Bethesda, Maryland, USA.
  66. Rausher MD (1992) The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 46:616–626CrossRefGoogle Scholar
  67. Reed DC, Foster MS (1984) The effects of canopy shadings on algal recruitment and growth in a giant kelp forest. Ecology 65:937–948CrossRefGoogle Scholar
  68. Rueffler C, Van Dooren TJM, Leimar O, Abrams PA (2006) Disruptive selection and then what? Trends Ecol Evol 21:238–245PubMedCrossRefGoogle Scholar
  69. Salles S, Aguilera J, Lopez-Figueroa F (1996) Light field in algal canopies: changes in spectral light ratios and growth of Porphyra leucosticta Thur. In Le Jol. Sci Mar 60:29–38Google Scholar
  70. Schluter D, Nychka D (1994) Exploring fitness surfaces. Am Nat 143:597–616CrossRefGoogle Scholar
  71. Schmalhausen II (1949) Factors of evolution: the theory of stabilizing selection. Blakiston, PhiladelphiaGoogle Scholar
  72. Schmitt J, Stinchcombe JR, Heschel MS, Huber H (2003) The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integr Comp Biol 43:459–469CrossRefGoogle Scholar
  73. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, SunderlandGoogle Scholar
  74. Scrosati R, DeWreede RE (1997) Dynamics of the biomass-density relationship and frond biomass inequality for Mazzaella cornucopiae (Gigartinaceae, Rhodophyta): Implications for the understanding of frond interactions. Phycologia 36:506–516CrossRefGoogle Scholar
  75. Silander JA (1985) Microevolution in clonal plants. In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 107–153Google Scholar
  76. Simms EL (1990) Examining selection on the multivariate phenotype: plant resistance to herbivores. Evolution 44:1177–1188CrossRefGoogle Scholar
  77. Starr RC, Zeikus J (1993) UTEX––The culture collection of algae at the University of Texas at Austin. J Phycol 29:1–106CrossRefGoogle Scholar
  78. Stanton ML, Thiede DA (2005) Statistical convenience vs biological insight: consequences of data transformation for the analysis of fitness variation in heterogeneous environments. New Phytol 166:319–338PubMedCrossRefGoogle Scholar
  79. Stearns S, de Jong G, Newman B (1991) The effects of phenotypic plasticity on genetic correlations. Trends Ecol Evol 6:122–126CrossRefGoogle Scholar
  80. Steinger T, Roy BA, Stanton ML (2003) Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis. J Evol Biol 16:313–323PubMedCrossRefGoogle Scholar
  81. Stewart HL (2006) Ontogenetic changes in buoyancy, breaking strength, extensibility, and reproductive investment in a drifting macroalga Turbinaria ornata (Phaeophyta) J Phycol 42:43–50CrossRefGoogle Scholar
  82. Thomsen MS, Wernberg T (2005) What affects the forces required to break or dislodge macroalgae? Eur J Phycol 40:139–148CrossRefGoogle Scholar
  83. Tuomi J, Vuorisalo T (1989) Hierarchical selection in modular organisms. Trends Ecol Evol 4:209–213CrossRefGoogle Scholar
  84. Van der Velde JT, King RJ (1984) The subtidal seaweed communities of Bare Island, Botany Bay. Wetlands 4:7–22Google Scholar
  85. van Kleunen M, Fischer M (2001) Adaptive evolution of plastic foraging responses in a clonal plant. Ecology 82:3309–3319CrossRefGoogle Scholar
  86. van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60PubMedCrossRefGoogle Scholar
  87. van Tienderen PH (1991) Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317–1331CrossRefGoogle Scholar
  88. Via S (1993) Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? Am Nat 142:352–365CrossRefPubMedGoogle Scholar
  89. Via S, Gomulkiewicz R, de Jong G, Scheiner SM, Schlichting CD, van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217CrossRefGoogle Scholar
  90. Via S, Hawthorne DJ (2005) Back to the future: genetic correlations, adaptation and speciation. Genetica 123:147–156PubMedCrossRefGoogle Scholar
  91. Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522CrossRefGoogle Scholar
  92. Viejo RM, Åberg P (2001) Effects of density on the vital rates of a modular seaweed. Mar Ecol Prog Ser 221:105–115CrossRefGoogle Scholar
  93. Weinig C (2000) Differing selection in alternate competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136PubMedGoogle Scholar
  94. Weinig C, Delph LF (2001) Phenotypic plasticity early in life constrains developmental responses later. Evolution 55:930–936PubMedCrossRefGoogle Scholar
  95. Weinig C, Johnston J, German ZM, Demink LM (2006) Local and global costs of adaptive plasticity to density in Arabidopsis thaliana. Am Nat 167:826–836CrossRefGoogle Scholar
  96. Witman JD, Dayton PK (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Press, Sunderland, pp 33–366Google Scholar
  97. Womersley HBS (1996) The marine benthic flora of Southern Australia. South Australia Government Printing Division, AdelaideGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Keyne Monro
    • 1
    Email author
  • Alistair G. B. Poore
    • 1
  • Robert Brooks
    • 1
  1. 1.School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia

Personalised recommendations