Institut für Evolution und Ökologie

Theme 3: Morphological variability in plants growing along steep and subtle environmental gradients - an evolutionary test of the stress gradient hypothesis

Bettina Springer
(K. Tielbörger, Co-supervisor: K. Harter)

In this subproject, we will test two primary hypotheses:

  1. The stress gradient hypothesis (SGH, see e.g. Bertness & Callaway 1994) applies independent of the intensity of stress and independent of species, i.e. positive interactions dominate stressful environments and vice-versa.
  2. Morphological variability is a good indicator for stress, i.e. plants become more asymmetric as stress increases and this is a phenotypic response to stress.


As case studies we use
a) an extreme gradient of aridity in Israel (see e.g. Holzapfel et al. 2004),
b) a less extreme gradient of nutrient availability and water availability in Germany (Swabian Alb), and possibly
c) a gradient of increasing temperature stress (frost) in the Bavarian Alps.


For the first two gradients, we have data on fitness response and morphological response of dominant plants species to increasing levels of resource limitation. Additional field work designed to evaluate symmetry (leaves and flowers) of most component species along the gradients and evaluation of variability of symmetry within populations allows to test the above hypotheses. The molecular basis of floral symmetry will then be evaluated in project no. 2. We predict decreasing asymmetry with increasing stress and increased symmetry within populations with neighbors under stressful conditions and vice-versa. Local adaptation to stress will be evaluated in a series of common garden experiments and via cross-transplants.

Key words: fluctuating asymmetry, stress gradient hypothesis, facilitation, competition

Literature

  • Alados, CL, Navarro, T, Escos, J, Cabezudo B & Emlen JM (2001) Translational and fluctuating asymmetry as tools to detect stress in stress-adapted and nonadapted plants. International Journal of Plant Sciences 162: 607-616
  • Arts M-JSJ, Schill RO, Knigge T, Eckwert H, Kammenga JE, Köhler H-R (2004): Stress proteins (hsp70, hsp60) induced in isopods and nematodes by field exposure to metals in a gradient near Avonmouth, UK. Ecotoxicology 13, 739-755
  • Badawi A, Schmiedl G, Hemleben Ch (2005): Impact of Late Quaternary Environmental Changes on deep-sea benthic foraminiferal faunas of the Red Sea. Mar Micropal 58, 13-30
  • Bergman A, Siegal ML (2003): Evolutionary capacitance as a general feature of complex gene networks. Nature 424, 549-552
  • Betz O, Köhler H-R (2008): die Evolution des Lebendigen. Attempto-Verlag Tübingen, 304pp.
  • Bertness, M. & Callaway, R.M. (1994) Positive interactions in communities. Trends in Ecology and Evolution 9: 191-193.
  • Botto-Mahan, C, Pohl, N & Medel, R (2004) Nectar guide fluctuating asymmetry does not relate to female fitness in Mimulus luteus. Plant Ecology 174: 347-352
  • Brooker, R.W. & Callaghan, T.V. (1998) The balance between positive and negative plant interactions and its relationship to environmental gradients: a model. Oikos 81: 196-207.
  • Brooker, R.E.; Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L., Kunstler, G., Liancourt, P., Tielbörger, K., Travis, J.M., Anthelme, F., Armas, C., Coll, L., Corcket, E., Delzon, S., Forey, E., Kikvidze, Z., Pugnaire, F., Saccone, P., Schiffers, K., Seifan, M., Touzard, B. & Michalet, R. (2008): Facilitation in plant communities: the past, the present and the future. Journal of Ecology 96: 18-34
  • Brose, U. & Tielbörger, K. (2005): Subtle differences in environmental stress along a flooding gradient affect the importance of interspecific competition in an annual plant community. Plant Ecology 178: 51-59.
  • Bubliy OA, Loeschcke V, Imasheva AG (2000): Effect of stressful and nonstressful growth temperatures on variation of sternopleural bristle number in Drosophila melanogaster. Evolution 54, 1444-1449
  • Callaway, R.M., Brooker, R.W., Choler, P., Kikvidze, Z., Lortie, C.J., Michalet, R., Paolini, L., Pugnaire, F.I., Newingham, B., Aschehoug, E.T., Armas, C., Kikodze, D. & Cook, B.J., (2002) Positive interactions among alpine plants increase with stress. Nature 417: 844-848.
  • Ceranka, T. 2007. Symmetry disorders of the test of the Miocene echinoid Echinocyamus from Poland. Acta Palaeontologica Polonica 52: 503–518.
  • Clarke GM. 1993. Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ. Pollut. 1993, 82, 207-11.
  • Dafni J (1980); Abnormal growth patterns in the sea urchin Tripneustes cf. gratilla (L.) under pollution (Echinodermata: Echinoidea). J. Exp. Mar. Biol. Ecol., 47:259-279
  • David B, Laurin B (1991); Shape analyses in echinoids. Scalera-Liaci, L. & Canicatti, C. (eds.) Echinoderm Research, Rotterdam, Balkema,11-16.
  • David B, Laurin B (1996): Morphometrics and cladistics: measuring phylogeny in the sea urchin Echinocardium. Evolution 50, 348-359.
  • Dimitriou I, Aronsson P, Weih M (2006) Stress tolerance of five willow clones after irrigation with different amounts of landfill leachate. Bioresource Technology 97: 150-157.
  • Dongen SV (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol. 2006. 19:1727-43.
  • Ebert TA (1988): Allometry, design and constraint of body and shape in sea urchins. Journal of Natural History 22, 1407-1425.
  • Frey, FM, Davis, R, Delph, LF (2005) Manipulation of floral symmetry does not affect seed production in Impatiens pallida. Inernational Journal of Plant Sciences 166: 659-662.
  • Geslin E, Heinz P, Jorissen F, Hemleben Ch (2004a): Migratory responses of deep-sea benthic foraminifera to variable oxygen conditions: laboratory investigations. Mar Micropal 53, 227-243
  • Geslin E, Heinz P, Hemleben Ch (2004b): Behaviour of Bathysiphon sp. and Siphonammina bertholdii n.gen n.sp. under controlled oxygen conditions in laboratory: implication for bioturbation. In: Bubik M & Kaminski MA (eds) 2004. Proceedings of the Sixth International Workshop on Agglutinated Foraminifera, Grzybowski Foundation Special Publication 8, 105-118
  • Grime, J.P. (1973) Competitive exclusion in herbaceous vegetation. Nature 242: 344-347.
  • Grime, J.P. (1974) Vegetation classification by reference to strategy. Nature 250: 26-30.
  • Grime, J.P. (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111: 1169-1194.
  • Gross O (2000): Influence of temperature, oxygen and food availability on the migrational activity of bathyal benthic foraminifera: evidence by microcosm experiments. Hydrobiologica 426,123-137
  • Gross O. (2002): Sediment interactions of foraminifera: implications for food degradation and bioturbation processes. J Foram Res 32, 414-424
  • Heinz P (2001): Laboratory feeding experiments: response of deep-sea benthic foraminifera to simulated phytoplankton pulses. Rev Paléobiol 20, 643-64
  • Heinz P, Schmiedl G, Kitazato H, Hemleben Ch (2001): Response of deep-sea benthic foraminifera from the Mediterranean Sea to simulated phytoplankton pulses under laboratory conditions. J Foram Res 31, 210-227
  • Heinz P, Hemleben Ch, Kitazato H (2002): Time-response of cultured deep-sea benthic foraminifera to different algae diets. Deep-Sea Res I 49, 517-537
  • Heinz P, Geslin E, Hemleben Ch (2005): Laboratory observations on benthic foraminiferal cysts. Mar Biol Res 1, 149-159
  • Heinzeller T, Nebelsick, JH (2004): Echinoderms München: Proceedings of the 11th International Echinoderm Conference. A.A. Balkema Publishers, Leiden. 633 pp.
  • Hemleben C, Kitazato H (1995) Deep-Sea foraminifera under long time observation in the laboratory. Deep-Sea Res 42, 827-832
  • Hendrickx F, Maelfait JP, Lens L (2003): Relationship between fluctuating asymmetry and fitness within and between stressed and unstressed populations of the wolf spider Pirata piraticus. J Evol Biol., 16, 1270-9.
  • Hoffmann AA, Merilä J (1999): Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14, 96-101
  • Hoffmann AA, Parsons PA (1997): Consistent heritability changes under poor growth conditions. Trends Ecol. Evol. 12, 460-461
  • Holzapfel, C., Tielbörger, K., Parag, H.A., Kigel, J. & Sternberg, M. (2006): Annual plant-shrub interactions along an aridity gradient. Basic and Applied Ecology 7: 268-279.
  • Horstmann H (2007): Is there facilitation in Central European grassland? A search for patterns. Diplomarbei, Universität Tübingen (unter Betreuung von K. Tielbörger).
  • Imasheva AG, Loeschcke V, Zhivotovsky LA, Lazebny OE (1997). Effect of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii. Biol. J. Linnean Soc. 61, 117-126
  • Köhler H-R, Eckwert H, Triebskorn R, Bengtsson G (1999): Interaction between tolerance and 70 kD stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution. Appl. Soil Ecol. 11, 43-52
  • Köhler H-R, Triebskorn R, Stöcker W, Kloetzel P-M, Alberti G (1992): The 70 kD heat shock protein (hsp 70) in soil invertebrates: A possible tool for monitoring environmental toxicants. Arch. Environ. Contam. Toxicol. 22, 334-338
  • Köhler H-R, Zanger M, Eckwert H, Einfeldt I (2000): Selection favours low hsp70 levels in chronically metal-stressed soil arthopods. J. Evol. Biol. 13, 569-582
  • Köhler H-R, Lazzara R, Dittbrenner N, Capowiez Y, Mazzia C, Triebskorn R (in press): Snail phenotypic variation and stress proteins: do different heat response strategies contribute to Waddington's widget in field populations? J. Exp. Zool. B
  • Körner, C. (2003) Limitation and stress - always or never ? Journal of Vegetation Science 15: 141-143
  • Körner, C. (2004) Individuals have limitations, not communities - A response to Marrs, Weiher and Lortie et al. Journal of Vegetation Science 15: 581-582
  • Kowalewski M, Nebelsick, JH (2003): Predation on recent and fossil echinoids. In Kelley PH, Kowalewski M, Hansen TA, eds., Predator-Prey Interactions in the Fossil Record: Topics in Geobiology Series, Plenum Press, Kluwer. 279-302.
  • Kristensen TN, Dahlgaard J, Loeschcke V (2003) : Effects of inbreeding and environmental stress on fitness – using Drosophila buzzatii as a model organism. Conservation Genet. 4, 453-465
  • Kroh A, Nebelsick JH (2003): Echinoid assemblages as a tool for palaeoenvironmental reconstruction - an example from the Early Miocene of Egypt. Palaeogeography, Palaeoclimatology, Palaeoecology. 157-177.
  • Kroh A, Nebelsick JH (in press): Echinoderms and Oligo-Miocene Carbonate Systems - Potential applications in sedimentology and environmental reconstruction. In Betzler C, Mutti M, Piller W (eds). Evolution of carbonate systems during the Oligocene-Miocene climatic transition. Special Developments in Sedimentology.
  • Kucera M, Widmark JGV (2000): Gradual morphological evolution in a Late Cretaceous deep-sea benthic foraminiferan, Parkiella. Historic Biol 14, 205-228
  • Lawrence JM, Pomory CM, Sonnenholzner J, Chao C-M (1998). Bilateral Symmetry of the Petals in Mellita tenuis, Encope micropora, and Arachnoides placenta (Echinodermata: Clypeasteroida) Invertebrate Biology, 117 (1), 94-100.
  • Lens L, Van Dongen S, Kark, S, Matthysen E (2002): Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol. Rev. Camb. Philos. Soc., 77, 27-38.
  • Liancourt P & Tielbörger K. (2009): Competition and a short growing season lead to ecotypic differentiation at the two extremes of the ecological range. Funct. Ecol 23: 397-404.
  • Lortie, C.J., Brooker, R.W., Kikvidze, Z. & Callaway, R.M. (2004) The value of stress and limitation in an imperfect world: A reply to Körner. Journal of Vegetation Science 15: 577-580.
  • Malkinson, D. & Tielbörger, K. (accepted): What does the stress-gradient-hypothesis predict? A plea for more thought. Oikos.
  • McKinney ML (1984) Allometry and heterochrony in an Eocene echinoid lineage: morphological change as a by-product of size selection. Paleobiology, 10, 407-419.
  • Maestre, F.T., Valladares, F. & Reynolds, J.F. (2005) Is the change of plant-plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments. Journal of Ecology 93: 748-757.
  • Mitchell-Olds T , Knight CA (2002): Evolution: chaperones as buffering agents? Science 296, 2348-2349
  • Moller AP, Shykoff JA (1999) Morphological developmental stability in plants: Patterns and causes. International Journal of Plant Sciences 160: S135-S146
  • Nebelsick JH (1992a): Components analysis of component distribution in Lower Miocene temperate carbonates of the Zogelsdorf Formation, Lower Austria. Palaeogeography, Palaeoclimatology, Palaeoecology, 91, 59-69.
  • Nebelsick JH (1992b): The use of fragments in deducing echinoid distribution by fragment identification in Northern Bay of Safaga; Red Sea, Egypt. Palaios, 7, 2, 316-328.
  • Nebelsick JH (1995a): The uses and limitations of actuoapalaeontological investigations on Echinoids. Geobios, M.S. 18, 329-336.
  • Nebelsick JH (1995b): Comparative taphonomy of Clypeasteroids. Eclogae geol. Helv. 88, 685-693.
  • Nebelsick JH (1995c): Actuopaleontological investigations on echinoids: The potential for taphonomic interpretation.- in - Emson RH, Smith AB, Campbell AC. (eds.): Echinoderm Research, 209-214, Balkema, Rotterdam
  • Nebelsick, J. H. 1996: Biodiversity of shallow-water Red Sea Echinoids: implications for the fossil record. J. mar. biol. Ass. U.K. 76, 185-194.
  • Nebelsick JH (1999a): Taphonomic comparison between Recent and fossil sand dollars. Palaeogeography, Palaeoclimatology, Palaeoecology , 149, 349-358.
  • Nebelsick JH (1999b): Taphonomic legacy of predation on echinoids. In Candia Carnevali MD, Bonasoro F. (eds.): Echinoderm Research 1998, 347-352. Balkema, Rotterdam.
  • Nebelsick JH (1999c): Taphonomic Signatures and Taphofacies Distribution as recorded by Clypeaster fragments from the Red Sea. Lethaia , 32, 241-252.
  • Nebelsick JH (2004): Taphonomy of Echinoderms: Introduction and Outlook. In Heinzeller T, Nebelsick, JH (eds): Echinoderms: München: Proceedings of the 11th International Echinoderm Conference. A.A. Balkema Publishers, Leiden. 471-484.
  • Nebelsick J.H. (2008): Taphonomy of Recent Clypeaster: Implications for fossil assemblages. In: Ausich, W. & Webster, G. (eds), Paleobiology of Echinoderms. Indiana University Press. 114-128.
  • Nebelsick JH, Kowalewski M (1999): Drilling Predation on Recent Clypeasteroid Echinoids from the Red Sea. Palaios , 14, 127-144.
  • Nebelsick, JH, Kroh, A (2002): The Stormy Path from Life to Death Assemblages: The Formation and Preservation of Mass Accumulations of Fossil Sand Dollars. Palaios, 17, 378-394
  • Nebelsick JH, Schmid B, Stachowitsch M (1997): The encrustation of fossil and recent sea-urchin tests: ecological and taphonomic significance. Lethaia , 30, 271 - 284.
  • Nomaki H, Heinz P, Hemleben Ch, Kitazato H (2005): Behavior and response of deep-sea benthic foraminifera to freshly supplied organic matter: a laboratory feeding experiment in microcosm environments. J Foram Res 35, 103-113
  • Oyen CW, Fuellhart KG (2004): Symmetry Patterns in selected fossil and Recent Mellitid echinoids: How much shape variation really exist. GSA 2004 Denver Annual Meeting (November 7–10, 2004). Abstract Paper No. 181-5.
  • Palmer, A.R. & Strobeck, C. 1986. Fluctuating Asymmetry: Measurement, Analysis, Patterns. Ann. Rev. Ecol. Syst. 1986. 17:391-421
  • Pelabon C, Hansen TF, Carlson ML, Armbruster WS (2006) Patterns of asymmetry in the twining vine Dalechampia scandens (Euphorbiaceae): ontogenetic and hierarchical perspectives. New Phytologist 170: 65-74
  • Petrů, M., Tielbörger, K., Belkin, R. & Sternberg, M. & Jeltsch, F. (2006): Life history variation of an annual plant under two opposing selective forces along a steep climatic gradient. Ecography 29: 66-74.
  • Pigliucci M (2005): Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20, 481-486
  • Queitsch C, Sangster TA, Lindquist S m(2002): Hsp90 as a capacitor of phenotypic variation. Nature 417, 618-624
  • Ruden DM, Garfinkel MD, Sollars VE, Lu X (2003): Waddington´s widget: Hsp90 and the inheritance of acquired characters. Sem. Cell Dev. Biol. 14, 301-310
  • Ruden DM, Xiao L, Garfinkel MD, Lu X (2005): Hsp90 and environmental impacts on epigenetic states: A model for the trans-generational effects of diethylstilbestrol on uterine development and cancer. Human Mol. Gen. 14, R149-R155
  • Rutherford SL, Lindquist S (1998): Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342
  • Sangster TA, Queitsch C (2005): The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr. Op. Plant Biol. 8, 86-92
  • Saucede T, Alibert P, Laurin B, David B (2006). Environmental and ontogenetic constraints on developmental stability in the spatangoid sea urchin Echinocardium (Echinoidea). Biological Journal of the Linnean Society 88 (2), 165–177..
  • Schiffers, K. & Tielbörger, K. (2006): Ontogenetic shifts in interactions among annual plants. Journal of Ecology 94: 336-341.
  • Schloz-Murer D (2005): Effect of small-scale disturbances on European grassland community dynamics along a productivity gradient: molehills as a case study. Diplomarbeit unter Betreuung von K. Tielbörger.
  • Schmid A (2006): Die Dynamic europäischer Wiesengemeinschften entlang eines Produktivitätsgradienten. Diplomarbeit, Universität Tübingen (unter Betreuung von K. Tielbörger und R. Hampp)
  • Schmiedl G, Mitschele A, Beck S, Emeis K-C, Hemleben Ch, Schulz H, Sperling M, Weldeab S (2003): Benthic foraminiferal record of ecosystem variability in the eastern Mediterranean Sea during times of sapropel S5 and S6 deposition. Palaeogeogr Palaeoclimatol Palaeoecol 190, 139-164
  • Schmidt DN, Lazarus D, Young JR, Kucera M (2006): Biogeography and evolution of body size in marine plankton. Earth Science Reviews 78, 239-266
  • Seifan, M., Tielbörger, K., Schloz-Murer, D., Seifan, T. (akzeptiert): Contribution of small-scale disturbances to grassland community composition along a productivity gradient – molehills as a case study. Acta Oecologica .
  • Seilacher A (1979) Constructional morphology of sand dollars, Paleobiology, 5, 191-221.
  • Sinclair, C. & Hoffmann, AA (2003) Monitoring salt stress in grapevines: Are measures of plant trait variability useful? Journal of Applied Ecology 40: 928-937
  • Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM (2003): evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nature Genetics 33, 70-74
  • Sperling M, Schmiedl G, Hemleben Ch., Emeis K-C, Erlenkeuser H, Grootes PM (2003): Black Sea impact on formation of eastern Mediterranean sapropel S1?: evidence from the Marmara Sea. Palaeogeogr Palaeoclimatol Palaeoecol 190, 9-21
  • Suzuki Y, Nijhout HF (2006): Evolution of a polyphenism by genetic accommodation. Science 311, 650-652
  • Tielbörger, K. & Kadmon, R. (2000a): Indirect effects in a desert plant community: is competition among annuals more intense under shrub canopies? Plant Ecology 150: 53-63.
  • Tielbörger, K. & Kadmon, R. (2000b): Temporal environmental variation tips the balance between facilitation and interference in desert plants. Ecology 81: 1544-1553.
  • Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution 16:125-142.
  • Waddington C (1942): Canalization of development and the inheritance of acquired characters. Nature 150, 563-565.