versus plasticity in clonal plant characteristics: when is
it good to adjust?
Peter Alpert, Department
of Biology, University of Massachusetts,
Amherst MA, USA.
Clonal plant species
differ greatly in architectural plasticity.
For example, some species vary the spacing between ramets
according to resource levels in the environment, whereas other
species do not. The architecture of some species changes more in
response to resource contrasts, the difference in levels of a
resource from one place to another, than in response to
individual resource levels or their mean value. Patterns of a
different clonal characteristic, resource sharing, may also be
more plastic in some species than in others, but this has been
less well studied. Illustrative data for the clonal herb
Fragaria chiloensis suggest that the amount of resource sharing
between ramets in this species responds both to resource
contrasts and to absolute resource levels. Recent models suggest
that the relative advantages of fixed versus plastic clonal
characteristics depend upon the spatial and temporal patterns of
resource heterogeneity in the habitat. Failure to respond to
environmental conditions or cues may reflect, not merely the
constraints of unsophisticated physiology, but selection for
conservatism. A comparative review of fixity versus plasticity
in clonal plant characteristics examines the hypothesis that
plasticity is advantageous when the plant can change faster than
the environment, disadvantageous when plant and environment
change at similar rates, and moot when the environment changes
faster than the plant.
Plasticity mechanisms: When the details matter.
Carlos L. Ballaré,
IFEVA, Dept. de Ecología, Facultad de Agronomía, Universidad
de Buenos Aires, Argentina.
Individual plants acclimate to (and sometimes anticipate) variations in their biotic and abiotic environment using a host of information-acquiring systems. These systems sense informational signals, activate the relevant molecular circuitry and ultimately elicit plastic changes in gene expression and protein function. Plastic responses are continuously implemented in the plant and serve a number of functions, including the maintenance of metabolic homeostasis, foraging for resources, and defense. In most cases plastic responses involve metabolic as well as morphological and developmental components. Therefore, classifying plants as plastic or non-plastic may be risky. Plants from harsh environments may show little morphological plasticity to, for example, light quality variations; however, chances are that they appear to be extremely plastic if one chooses to look at their metabolic responses to rapid variations in nutrient availability.
Although it is not uncommon in ecology textbooks to describe plant responses to environmental stresses as inevitable consequences of limitations or imbalances in the resources available to the plant, it is seldom pointed out that these responses are based on finely-tuned and coordinated information-transduction cascades, and do not necessarily represent the only possible solution to the resource conflicts presented by the environment. Plastic responses are triggered by a variety of signals, including things that are frequently considered only in terms of their energetic value or deleterious effects. Thus, signals that engage specific response programs include: (1) specific external clues (such as changes in the red:far-red ratio, biotic elicitors, etc.), (2) variations in the amount of resources available to the plant (e.g., incident PPFD, hexose level in a particular tissue, etc.), and (3) products of cellular damage (e.g., DNA lesions, free radicals, etc.). Any molecular mechanism that is capable of extracting information from 1, 2, and 3, and transforming that information into a potentially useful plastic response, should be expected to be under continuous selective pressure.
There is growing evidence indicating that different environmental and biotic factors can induce convergent information-transduction chains, which lead to similar plastic responses. For example, plastic responses to several stress factors (chilling, UV, water stress) may involve free radicals as messengers and result in the induction of antioxidant enzymes and enzymes of the phenylpropanoid pathway. It is therefore at least possible that a good part of the molecular circuitry that allows the plant to acclimate to fluctuations in a given environmental factor may have been selected under the combined influence of various environmental factors.
Frequently, the functional details of the mechanisms that allow plants to sense and react plastically to changes in their environment tend to be ignored or overlooked in descriptions of plant responses to competition or to abiotic stresses. Some of the limitations associated with the use of very simple models of plant function will be discussed. For example, it is clear that competition models that are simply based on resource consumption cannot account for plastic, active morphological responses of the plants, which in many environments are critical for the outcome of competition. Similarly, the lack of a mechanistic description of plastic responses to environmental factors will make it difficult to understand why there is cross-acclimation to disparate stress sources, and will certainly limit our ability to design fruitful experiments to understand how plants cope with environmental variation.
Experimental Evolution of Plasticity and Diversity
Graham Bell, Department of Biology, McGill University, Montreal, Quebec, Canada.
The evolution of specialization
and generalization is determined by how
fitness varies with circumstances. This is most conveniently studied in
microbes, and the unicellular green alga Chlamydomonas is an appropriate
model organism. Simple pure-culture trials have shown that
genotype-environment interaction constitutes a large part of the overall
variation of fitness. Genotypes and species vary in how much
environmental variance they express, and in their relative fitness in
different environments. Moreover, the genetic correlation of fitness
falls as the difference between environments increases, and also as the
distance between genotypes increases. Thus, diversity rather than
plasticity is expected to prevail when types that are sufficiently
well-differentiated compete in an environment that is sufficiently
heterogeneous. These conclusions were tested in selection experiments
contrasting the fate of genetic variation in uniform and heterogeneous
environments in the laboratory. In experiments with a single species,
selection in heterogeneous environments permitted higher levels of
genetic variance to be maintained. This was because divergent selection
in strongly contrasted environments tended to be anticlinal, with
adaptation to one environment resulting in a loss of adaptation to
another environment. When the environment varied through time, however,
generalization evolved. Comparable experiments with a set of distantly
related species of soil algae gave different results, apparently because
strong biotic interactions in mixtures overwhelmed differences in the
rates of growth in pure culture.
and pulses: Exploitation of soil resources by roots of
Martyn M. Caldwell,
Dept. Rangeland Resources and the Ecology Center,
Utah State University, Logan, Utah, USA
An appreciable focus
on soil spatial heterogeneity and plant root
response to resources patchiness has been evident in the literature of
the past decade. Soil heterogeneity can be statistically as large
within the span of a single plant root system as in the entire
vegetation stand. Clearly, roots often proliferate in rich soil patches
in many experiments, by branching and sometimes by increased specific
root length. However, a distinct correlation between root mass and soil
nutrients in the field is often not apparent. Model simulations drawing
upon several years of data on soil patchiness, root proliferation and
root physiological uptake kinetics behavior of species growing in these
soils indicates the particular importance of adjustments in uptake
kinetics in many situations. Also, shading can dampen the capacity to
elevate root uptake kinetics in rich soil patches. For phosphate-rich
patches, mycorrhizae have been demonstrated to facilitate patch
exploitation. Though often mentioned in the literature, there is but
scant information to characterize temporal variability of soil nutrient
resources in nonagricultural ecosystems. It appears that soil inorganic
nitrogen pools can turnover very rapidly and temporal variability in
available nitrogen is likely to be quite sizeable. Also precipitation
events following prolonged dryness often result in the release of
available nitrogen. Field studies of six species of different life form
indicated a remarkable capacity by most species to capture very brief
pulses of nitrogen. These plants could acquire more nitrogen from a
distinct four-day pulse than from controls in which the same quantity of
nitrogen was evenly delivered over a 10-week period. However, timing of
the pulse was critical and species differed in regard to the optimum
time for exploiting nitrogen pulses. This capacity was apparently not
linked to elevated uptake kinetics. However, the ability of plants to
capture a nitrogen pulse following wetting of very dry soil, was linked
to elevated uptake kinetics. The role of hydraulic lift in facilitating
nutrient pulse acquisition will be discussed.
The Evolution of Adaptive Responses in Plants: Phenotypic Flexibility, Individual Learning, and Population Interactions
Dan Cohen, Department
of Evolution, Systematics and Ecology, The Silberman Institute of Life
Sciences, The Hebrew University of Jerusalem, Israel.
Current address: Center for Computational Genetics and Biological Modeling,
Stanford University, Stanford CA, USA.
The evolution of three
types of adaptive strategies in plants is modeled for
different types of activities and developmental processes:
1. Fixed developmental programs, that are insensitive to a wide range of external or
internal changes or perturbations.
2. Genetically pre-programmed phenotypic adaptive responses, without
feedback (learning) from the consequences of the responses.
3. Individual modifications of the adaptive responses by positive or negative
feedback or reinforcement by the consequences of the response or the action, i.e.
1.1 Selection modifies
the responses to proximal signals to maximise the
expected fitness caused by the interaction of the responses with the ultimate
factors. The effectiveness of the signals depends on the degree to which they are
correlated with the subsequent outcome.
1.2 Phenotypic flexibility
is selected for in all cases when individuals in a
population are exposed to different unpredictable environmental conditions.
The selective advantage of phenotypic flexibility decreases relative to
genetic determinism by:
a. Increased predictability of environmental conditions and changes.
b. Increased costs of perception and processing of the signals and of the
c. Decreased availability of effective correlations and signals.
1.3 Selection favours fixed phenotypic responses, without feedback and
learning, if there is a strong positive correlation between the optimal responses
of different individuals that have been exposed to similar events.
Selection favours a conditional phenotypic flexibility with feedback and
learning, if there are weak or negative correlations between the optimal
responses of different individuals that have been exposed to similar events.
However, a fixed phenotypic response without feedback and learning is
selected for if the consequences of the responses are too remote in time, or the
events too rare, to allow the learning of the association between the signals, the
responses, and their consequences.
2. The evolution of
adaptive responses with feedback (Learning):
Learning in plants may be defined as the genetically programmed
modification of changes of development in response to a stimulus or a situation,
by an association between negative or positive reinforcement feedback and the
response or action. Positive reinforcement increases the intensity and/or the
probability of the response or action, while negative reinforcement has the
opposite effects of decreasing the intensity and/or the probability of the
We assume that the evolution of learning responses have caused the
consequences of responses that are positively correlated with an increase in
fitness to act as positive reinforcement, while the consequences that are
negatively correlated with the change in fitness cause a negative reinforcement.
3.1 The number of exposures
increases the strength of an association between an
event, a response, and the reinforcement, which provides positive reinforcement for investing time and effort in collecting more information.
3.2 More information
becomes available during development, because the temporal
correlation structure of the environment is usually stronger, and the internal uncertainties within each individual usually decrease for shorter time intervals. Thus, reinforcement and the associated fitness would increase by collecting more information and delaying the decisions.
4. There are two main
constraints for using information in development:
4.1 The constraint of developmental time: e.g. many developmental processes have to be implemented at some early stages of development, with much important
information still missing.
4.2 The constraint
of developmental irreversibility: development of an individual
usually includes irreversible developmental processes. Thus, the decisions at some early stage necessarily constraint the future development of that individual at later stages.
Representative examples of the three types of strategies are discussed.
The nature of morphological plasticity in clonal plants and its implications
Hans de Kroon1
and Jan van Groenendael2,
1Department of Terrestrial Ecology and Nature Conservation, Agricultural University, Wageningen, 2Department of Ecology, University if Nijmegen, Nijmegen, The Netherlands.
The length responses of clonal spacers such as rhizomes and stolons are
discussed as examples of morphological plasticity. Manipulative experiments
show that the phenotypic expression of spacer length is the result of an
inherent developmental plan in interaction with the environment. The very
nature of the developmental pattern may result in considerable developmental
noise (non-plastic variation) which constrains the occurrence of plasticity.
As a rule, plasticity in spacer length and other forms of morphological plasticity in clonal plants are expressed within a single genetic and physiological individual. Plastic responses by ramets may be enhanced if they are interconnected to ramets of the same clone that experience other conditions. There are even examples that show that local morphological responses occur in integrated clonal individuals only, so that the occurrence of plasticity is confined to a single individual. As clonal individuals are long-lived they are likely to experience a variety of conditions throughout their life-time. Plastic adjustments in morphology are ubiquitous throughout, and are likely to play a crucial role in the persistence of clones.
The picture that emerges is one of morphological plasticity as a prevalent feature of the life history of clonal plants, constrained by the developmental plan of the species. The implications for the evolution of plasticity are discussed. The evolutionary theory of plasticity as developed for unitary animals may not apply to clonal plants or even to all plants as modular sessile organisms.
Trait plasticity and resource availability: a comparative analysis
Andrew R. Dyer1,
Roy Turkington2, Deborah E. Goldberg1, and Cindy
1Department of Biology, University of Michigan, Ann Arbor, Michigan, USA,
2Department of Botany, University of British Columbia, Vancouver, Canada
Does plasticity vary
in consistent ways among types of traits, types of
species, and types of environments, or in complex ways involving all three?
Recent efforts comparing large numbers of species from one or more source
environments have focused on traits measured in a single, generally
favorable, growing environment. However, plasticity in many traits has been
predicted to change in consistent ways among environments and such changes
have important implications for species competitive ability. We tested
these predictions with data collected from 47 species (13 grasses and 34
dicots) in two stabilized sand-dune communities from either end of a
rainfall gradient in a Mediterranean climate extending from a wet coastal
site to a drier mid-desert site. Using standard protocols (Hendry and Grime
1993), plants were grown under either high resource conditions (nutrients
and high water) or low resource conditions (no nutrients and low water) and
harvested 7 and 21 days after emergence.
and univariate techniques, we found strong and repeated
differences between the two environments for both single traits and sets of
traits. Plant functional groups were clearly identified and were
characterized not only by grasses and dicots, but also by environment. The
functional groups were consistent at Day 7 regardless of growing conditions,
but group identity diverged between treatments by Day 21. Measures of
plasticity, either for species or for traits, varied considerably across
treatments, but the species from the coastal environment generally showed a
greater range of response as well as larger mean values.
These results support
theoretical expectations that species from harsh and
low productivity environments should exhibit more conservative expression of
traits than species from more predictable and mesic environments. Also,
while traits are correlated with adaptive characteristics of plants, these
data suggest that plant functional group identities and species traits are
based on seedling processes and characteristics that are both plastic and
Respiration; an indicator of feed-forward adaptative response
of Plants to Stress
Joe Gale and Jossy Reuveni, Dept. of Plant Sciences, The Hebrew University of Jerusalem, Israel
Low level stress, such as from salinity, heat or pathogens, has been reported to increase plant tolerance to later exposure to higher stress levels. This is often correlated to an increase in dark respiration.
Suppression of dark respiration, by high concentrations of ambient carbon-dioxide, sometimes increases carbon gain, in low stressed plants. However, we have found that this suppression is followed by a reduced tolerance of subsequent, higher levels of stress.
It is tentatively concluded that the increased rate of dark respiration (especially maintenance respiration) measured in low stress challenged plants, is a result of the induction and maintenance of energy-consuming, feed - forward, stress adaptation mechanisms.
plasticity in pea roots (Pisum sativum L.) exposed to
Mordechai Gersani & Omer Falik, Department of Life Sciences, Ben-Gurion University of the Negev, Israel.
Habitat selection in
plants is a prolonged process that lasts a number of
generations and includes in it the component of seeds dispersal. In the
present study, an attempt was made to demonstrate habitat selection as a
result of heterogeneous environment during lifetime of a non-clonal annual
plant. The study hypothesis assumes that the attribute of phenotypic
plasticity of plant may greatly compensate its lack of mobility for
assessment and preference of habitat selection. A split root system of pea
plant, called "fence-sitter", was chosen to demonstrate its response to
intraspecific competition with other pea plants. The root system was
divided in two different compartments: in one, the split root
was exposed to intraspecific competition with roots of 1-4 plants, while in the counterpart compartment the root was free from competition. We also run experiments in which both root were exposed to 1-4 competing roots.
When one pot was free
of competition, the total root biomass and the
fitness (measured by the dry fruit biomass) of the fence-sitter decreased only
slightly and insignificantly in response to increased density of competitor plants. When competition was present in both sides of the fence-sitter, the total root biomass and the fitness of the fence-sitter was inversely proportional to the root biomass of the competitor plants.
The success of the fence-sitter plant to reach high constant fitness can be explained by the plastic distribution of the roots according to the density of competing roots. It can be concluded, therefore, that plastic development allow pea plants demonstrate a micro-habitat selection.
Plasticity as a determinant of community patterns, and environmental and evolutionary constraints on plasticity
Thomas J. Givnish, Department of Botany and The Institute for Environmental Studies, University of Wisconsin, Madison WI, USA.
species or guilds in their patterns of developmental plasticity can limit
their ecological and geographic distributions as much as average differences
in the expression of specific traits. A case in point involves the
depth zonation of aquatic plants. In ponds, small lakes, and slow-moving
around the world, emergent plants dominate shallow water, floating-leaved plants dominate deeper water, and submersed plants dominate deeper water yet. This classic community pattern appears explicable in terms of differences between growth forms in competitive ability, allometric variation in allocation to petiole
vs. lamina, and ability to maintain a positive carbon balance at different depths. The different patterns of petiolar plasticity in emergent and aquatic plants appear adapted to the different mechanical stresses (compressive vs. tensile) each growth form experiences, and appear to generate fundamental gradients in the structure and composition of aquatic communities.
Evolution should shape
the extent of plastic variation in specific traits in response to several
factors (e.g., patterns of spatio-temporal variation in environmental conditions,
costs of sensory modalities for different cues, energetic costs of trait
modification). Traits with low costs of modification (e.g., stomatal conductance) should vary over short temporal intervals, while those with high costs of modification (e.g., organ construction) should vary over much longer periods. Low resource levels - caused by dense shade, poor soil, or chronic drought - may
strongly limit plant plasticity by favoring long leaf life-spans. Within an environment, selection should favor developmental programs that rely on the number of sensory modalities that maximize the difference between gross carbon uptake and the costs of maintaining and integrating the output of those modalities. Given that (i) a plant's optimal behavior will, in general, depend on several
different environmental parameters; that (ii) these parameters will often show strong correlations with each other over small portions of the earth's surface; and that (iii) such correlations will disappear or reverse themselves elsewhere, selection for optimal control of development in a particular range of environments will necessarily bring with it constraints on the ability to evolve patterns of plasticity that are appropriate elsewhere. This limit on plasticity (and, ultimately, on a species' ecological and geographic distribution) is distinct from previous ideas based on
cybernetic cost, gene flow, and spatial variation in selection pressures.
Dependence on particular signals or cue correlations may show little evolutionary lability within lineages. Congeneric species of forest herbs, for example, show little variation in leaf or floral phenology; the high cost of leaf and stem construction, together with seasonal variation in photon flux density, may be responsible for the origin of several phenological guilds on fertile sites, and the exclusion of all but those with those most long-lived leaves on infertile sites. Studies of adaptive radiation should include common-garden experiments, to ascertain that phenotypic differences between species in different ecological roles reflect genetic differences, not a shared pattern of developmental plasticity in the face of different environments.
An Evaluation of Traits That Potentially Limit the Geographic Expansion of Cocklebur (Xanthium strumarium)
Timothy Griffith, Department of Biology, Indiana University, Bloomington, Indiana, USA.
have long faced the problem of why the
geographic ranges of species are evolutionaraly constrained. However,
before existing hypotheses can be tested, the phenotypic changes needed in
order for individuals to survive and reproduce beyond the current range
limit must be identified. Here I present a conceptual framework for
identifying these phenotype changes and apply it to the common crop weed
Xanthium strumarium (cocklebur).
As a species evolves across an environmental gradient, a trait
value may need to either a) remain at some constant, optimal value in
order to maintain relative fitness (an essential trait) or b) evolve
different values in order to hold the essential trait value constant (a
response trait). These essential and response traits are likely to
constitute the traits that must either remain constant or change
respectively at the margin of a population if the species is to extend its
Optimal allocation theory provides a potential set of both
essential and response traits. The optimal ratio of vegetative allocation
at the time of first flower to final reproductive allocation is one
possible essential trait. Conversely, if reproductive allocation to all
fruits is simultaneous, the amount of time or number of degree days
required for fruits to mature may represent a different essential trait.
Pre-flowering growth rate, the time of the developmental switch from
vegetative to reproductive allocation and emergence and senescence dates
are possible response traits for these essential traits.
Previous studies of cocklebur and other plant populations along an
environmental gradient have suggested that ecotypic adaptation has
occurred and that it has often involved phenological changes, a result
consistent with the proposed essential and response traits important in
optimal allocation theory. I performed a reciprocal transplant experiment
to determine which if any of these essential and response traits might be
range limiting traits of cocklebur.
Phenotypic plasticity in plants; consequences for community and ecosystem function
Philip Grime, Unit of Comparative Plant Ecology, University of Sheffield, Sheffield, UK.
In this symposium and
in science at large, plant biologists are pursuing studies of plasticity
with many different objectives in view. Even among the ecologists,
there are differences in the scale of enquiry. However, as the fund
of information on plasticity grows there is an increasing possibility that
this can provide the basis
for predictions of the role of plasticity in community and ecosystem processes. This represents a potentially important step because for many ecologists (as distinct from evolutionary biologists) the defining challenge for our discipline remains that of developing testable predictions with respect to large-scale patterns and
The objective in this presentation will be to review the insights available from an unpublished comparative database on the plasticity of roots and shoots of forty-three widely-contrasted vascular plant species. The results suggest that used in conjunction with other standardised data, measurements of the scale, precision and rate of plastic responses can provide the basis for 'scaling-up' to plant community and ecosystem properties and responses to perturbation.
plasticity of seed "readiness to germinate" in plants occurring
Yitzchak Gutterman, The Jacob Blaustein Institute for Desert Research and the Department of Life Sciences, Ben-Gurion University of the Negev, Sede Boker Campus, Israel.
The most important
survival strategies of many plant species that occur in
extreme deserts are involved in mechanisms which ensure that after one rain
event only a small portion of the large seed banks of the plant species
will be "ready to germinate", even under optimal conditions of water,
temperature and other environmental factors. The risk to species survival
is thus reduced in the frequent occurrences of a long period of drought
following a period with optimal conditions for germination, as only a small
portion of the species' seed banks will be lost.
The main factors which may affect seed readiness to germinate in
many species can be separated into eight main groups, according to the
environmental factors during the developmental stages of the seeds, seed
position during maturation and in the dispersal unit. Other influences are
post maturation temperatures and seed age, or the local factors in the
microhabitat during the germination process.
1. Environmental factors, such as daylength and temperatures during seed
development and maturation which affect the plasticity of seed germination.
2. Phenotypic plasticity according to seed position in the fruit, on the
inflorescences or on the plants, during maturation.
3. Regulating mechanisms of synaptospermy and seed dispersal.
4. Post maturation factors, such as temperatures affecting afterripening.
5. Environmental factors during wetting, such as quantity of rain and
6. Time of the day or night of the beginning of a rain event that engenders
germination as a regulating mechanism for seeds requiring light or dark for
7. Regulating germination mechanisms in dispersal-units affected by seed
position and location of inhibitors.
8. Local desert soil as substrates with mechanical and biological
regulators for seed germination, according to the average annual rainfall
gradient in a particular area, which affect the soil micro-flora and soil
The phenotypic plasticity in the most common species reduces the
risk to survival as a smaller percentage of seeds from the larger seed
banks germinate in the right microhabitat after a suitable rain event.
Spatiotemporal heterogeneity in a mountain grassland and the plastic response of Festuca rubra
Tomas Herben1, Beata Oborny2 and Sylvie Pechackova1
of Botany, Academy of Sciences of the Czech Republic, Pruhonice,
2Dept. of Plant Taxonomy and Ecology, Eotvos Lorand University, Budapest, Hungary.
The existence and degree of plasticity makes sense only in relation to the structure of the environment, which is conventionally formalised as the spatial (vertical or
horizontal) and temporal distribution of patches of different environmental quality. Grasslands form structures which are patchy at the fine scale; this patchiness is largely caused by the presence of the species themselves, and therefore itself has a rather high rate of change in time. We used a clonally growing grass species, Festuca rubra, in a mountain grassland, as a model system to examine the field relevance of the plastic response of clonal growth to the quality of the local environment.
* Festuca rubra forms
both rather compact tussocks of ca. 10-20 tillers and also rather loose
tussocks. These growth forms are associated with different morphology at
the level of tillers (daughter shoots are formed intravaginally vs. extravaginally,
rhizomes are present or absent). Existing data suggest that these growth forms may be environmentally induced.
* These grasslands
have a fine-scale spatial structure (expressed by the structure of spatial
autocorrelations) and this structure itself changes in time. The environmental
grain (ranges of the spatial autocorrelations) is commensurable with
the growth rate and the tussock diameter of F. rubra.
We wanted to know whether
* F. rubra tussock density may be a plastic response to local environmental heterogeneity due to neighbour presence and density around the tussocks.
* Under which types of environmental spatio-temporal structures the plastic growth would be favoured relative to the non-plastic behaviour?
Therefore, we collected information on
* Horizontal spatial light distribution in the system and its relation to density of individual plant species and to overall abobeground biomass in the field.
* Plant response to the light levels observed in the field (in a growth chamber).
A population of clones
sampled in the field were used to assess the natural variation in the traits
associated with the tussock growth form. There was a strong plastic response
in the rhizome lengths and in the tussock density; there was also a GxE
interaction in the tussock density.
* Plant response to field conditions using implant experiment. Plants multiplied in culture were implanted back to their original locality to sites that differed in differed in species that were present as neighbours, in densities of these species and in fertilisation levels. Four clones were used to assess variation in the response between genotypes. Again, there were both overall plastic responses and a GxE interaction in the tussock density.
* A (strategic) spatially extended model is being built to determine which (and to what extent) spatio-temporal structures of the environment favour the plastic types compared to non-plastic ones.
Differential costs & benefits of plasticity in vertical and horizontal spacers
Heidrun Huber, Department
of Plant Ecology & Evolutionary Biology, Utrecht University, The Netherlands.
Closely related plant species may produce erect (vertical) or
stoloniferous (horizontal) shoots, respectively. Examples for this
phenomenon come from many plant genera including Potentilla,
Trifolium, Ranunculus, and others. As a consequence, stem inter-
nodes in erect species are oriented vertically, while the
homologous organs of their stoloniferous relatives (i.e., stolon
internodes) are oriented horizontally. Conversly, petioles of
creeping species are vertically oriented, while petioles of erect
species are usually not. In other words, homologous spacers (i.e.,
stem internodes, petioles) have a fundamentally different spatial
orientation in clonal and in erect species, and therefore they are
also likely to fulfil different ecological functions, and to
respond differently to environmental signals.
Plastic changes in the length of vertical structures is
thought to promote light capture in shade-avoiding species, by
shifting leaf blades in upper parts of the canopy. This ecological
function is fulfilled by different organs in erect and in
stoloniferous species. This leads to the question whether
homologous (i.e., developmentally similar) or analogous (i.e.,
functionally similar) spacers show equivalent degrees of shade-induced
plasticity in clonal and in erect species, respectively.
The latter would imply selection for changed degrees of plasticity
during the transition from the erect to the clonal growth habit,
and/or vice versa. It would further suggest differential costs and
benefits of plasticity in spacer length in these two groups of
To answer this question, 9 pairs of herbaceous species, each
comprising an erect and a closely related stoloniferous species,
were studied in a greenhouse experiment. Individuals of each
species were grown in simulated canopy shade (PPFD: 24%; r/fr-ratio:
0.2) and in full day light (PPFD: 100%; r/fr-ratio: 1.1),
respectively. The length and investment patterns of internodes and
petioles were measured after 5 weeks of growth.
Internodes and petioles of erect and stoloniferous species
responded in a consistently different way to shading. Vertical
spacers (i.e., internodes of erect & petioles of clonal species)
showed high degrees of phenotypic plasticity in their length, while
horizontal spacers (i.e., internodes of clonal, petioles of erect
species) hardly responded to shading in most species pairs. Plastic
increases in spacer length was positively correlated with increases
in spacer weight, which is interpreted as a clear cost of the
expression of plasticity. It is suggested that differences in
plasticity between vertically and horizontally oriented spacers is
related to the degree of environmental predictability.
The configuration of resource supply, plasticity and plant growth
Michael J. Hutchings, School of Biological Sciences, University of Sussex, Falmer, Brighton, Sussex, UK.
Resource distribution is spatially and temporally heterogeneous in all natural habitats, and heterogeneity can have a variety of forms. The impact of heterogeneity on plants depends on the form in which it is presented, and this talk will draw on experimental results to demonstrate that some forms of heterogeneity are more "visible", and provoke much larger plastic responses from plants, than others.
The effects of providing fixed quantities of resource in different spatial and temporal configurations will be discussed using results from experiments on both clonal and non-clonal species. It will be shown that, in heterogeneous environments, both local and whole-plant responses in the clonal herb Glechoma hederacea (Lamiaceae) are sensitive to the scale of patches of different quality, and to contrast in patch quality. This is manifested in (i) differences in the ability of the species to preferentially exploit the better quality patches of the environment, (ii) localised differences in morphology, reflecting differences in resource-acquisition activities which are related to local resource availability, (iii) ontogenetic changes in the development of modules. These phenomena culminate in wide variation in whole-clone yield between treatments despite the provision of identical quantities of resources in all cases. Comparisons of clone growth in environments providing the same quantity of resource overall, but with different degrees of contrast between good- and poor-quality patches, show that as contrast declines, greater use is made of the poor-quality patches of the environment. This is accompanied by a reduction in the extent to which localised differences in morphology are expressed. The effects on morphology and yield of several non-clonal species, when a fixed quantity of resource is provided in pulses which differ in duration and frequency, will also be discussed.
Patterns of phenotypic plasticity in rhizome and stolon development
Jaime Kigel, Department of Agricultural Botany, Faculty of Agricultural, Food and Environmental Sciences, the Hebrew University of Jerusalem, Rehovot, Israel.
Vegetative spread and reproduction by rhizomes and stolons shows a wide spectrum of developmental plasticity. It varies from fixed patterns of development that result in specific, stable plant architectures, to plastic patterns in which the developmental decision to produce rhizomes and stolons is the balanced outcome of interaction between intra-plant controls of development and environmental signals. Modulation of this plasticity can be realized at different stages of rhizome and stolon development:
a- during initial stages of axillary bud growth: early and autonomous determination of bud fate vs. labile patterns of bud development influenced by the environment.
b- at later stages
of growth, involving shifts in rhizome and stolon responses to environmental
cues, with concomitant changes in their geotropism and morphology.
The ability to respond to the environmental signals that induce these changes is species specific: it depends on the flexibility of the plant’s development program and is controlled by correlative processes within the plant. Three patterns of rhizome development, differing in their plasticity, will be presented as case studies:
1- the developmental plan for rhizome production and shoot growth is predetermined and independent of the environment (autonomous development). The case of Ruscus hypophyllum L..
2- Inherent positional morphogenetic gradients within the individual shoot determine the fate of its axillary buds, i.e. to develop into an erect shoot or a rhizome. Basal, first activated buds develop into rhizomes. The positional gradient also regulates the competence of the ensuing rhizome to respond to environmental or endogenous signals affecting its transition into an erect shoot. Developmental plasticity of the rhizome is modulated by temperature. The case of Sorghum halepense (L.) Pers.
3- The developmental program for rhizome and stolon production is very plastic. The resulting plant architecture is determined mainly by variation in environmental conditions. Transition forms between rhizomes and stolons are frequent. The case of Cynodon dactylon (L.) Pers.
The adaptive value of these patterns of rhizome and stolon development will be discussed in terms of timing of resource allocation to clonal vs. seed reproduction, and as a function of temporal habitat stability and spatial heterogeneity.
a population during synchronized development affects dry matter
allocation - comparison of a corn species with a below-ground storer
Dieter Schmitt2, Markus Schreiber2 and Diethard
für Botanik und Botanischer Garten, Universität Hohenheim, Germany
2Institut für Botanik, Technische Universität Darmstadt, Germany.
3Institut fur Umweltwissenschaften der Universitat Zurich, Switzerland.
The effect of successive release from intraspecific competition by thinning
was studied in the two different growth forms of herbs, the annual oat
species Avena sativa L. (cultivar "Erbgraf"), and the annual Raphanus
sativus L. var. sativus (radish, cultivar "Cherry Bell"). While Avena
allocates carbohydrates into grain filling in the reproductive phase,
Raphanus especially supports a hypocotyl as storage organ from the
vegetative phase onwards. Therefore, thinning should have entirely
different effects on the species-specific allocation patterns.
Avena was sawn at a density of 400 plants m-2 in 9m x 9m
field plots. I a
randomized design the plots were thinned in parts of the plots at the
vegetative and flowering stage to give densities of 100 plants m-2 and 25
plants m-2; thus, competition was released at different times and to
different degrees. Thinning did neither vary the number of flowers per
spikelet nor the number of panicles per shoot or the number of seeds per
plant at both times. In contrast, total leaf area, above-ground dry matter,
plant height, number of shoots per plant and total yield per plant was
strongly affected. Early thinning increased the number of shoots per plant
and above-ground dry matter in comparison to the unthinned control, but
reduced total leaf area and the number of flowers per nodium, whereas later
thinning increased the total yield per plant through an increased
individual grain weight. However, thinning to 25 individuals m-2 did
actually reduce growth and yield.
Raphanus seeds were germinated and 35 seedlings were planted into
sand-filled containers, each, at a density of 455 plants m-2 and 4.8 cm
between each individual. At day 22 and at day 31 after germination the
populations in some of the 40 containers were thinned to 156 plants m-2,
providing the remaining plants with double space in all directions.
Untreated containers were harvested over the period of cultivation, some at
the same time as thinning trook place. After 50 days all plants were
harvested. Statistical tests revealed a striking significance of the
influence of early thinning on hypocotyls as well as on leaves, whereas
effetcs of late thinning were low. An almost linear weight gain over time
was observed in the hypocotyl until final harvest, whereas other organs
declined. This was furthermore supported by early release of competition,
indicating that the hypocotyl is a high-priority organ for allocation.
Comparing both species indicates the significance of the time of thinning:
While for Avena, thinning in the generative state is more favourable to
achieve higher seed weight per plant, Raphanus profits of thinning in the
early vegetative state by promoting the growth of leaves, and, therefore,
improving yield of the hypocotyl.
Evaluating adaptive plasticity:
considerations in a phylogenetic
Martin J. Lechowicz, Department of Biology, McGill
Montreal, Quebec, Canada.
We can evaluate the generality and adaptive value of plastic
responses to an environmental change by comparisons among species set
in their phylogenetic context. For a particular phenotypic response
to environmental differences to be considered adaptively plastic that
response should 1) make functional sense and 2) be phylogenetically
structured. In other words, plastic changes among a set of
functionally related traits that enhance or at least sustain plant
performance in a new environment can be seen as adaptive plasticity,
especially if closely related species either behave similarly, or
diverge in ways that are consistent with a functional and
evolutionary trend in the phylogeny.
In this perspective, I evaluate the adaptive value of
diverse species of forest maples (Acer) that have been growing in
the simulated shade of a forest understory but then find themselves
in a sunnier environment with the death of an overstory tree. This
eventuality is commonplace in the ecology of all these maple species
and we can expect them to have evolved adaptations to both the
understory and the gap environments. Some sort of ecological and
evolutionary patterns should emerge in a comparison of the responses
of these forest maples to this natural transition from shaded to
arise in a review of a wide range of
ecophysiological and architectural responses of these maples to the
shade to sun transition:
1. Patterns of plasticity in functionally important traits
closely related species can be quite disparate. What appears to be
adaptive plasticity for one species, may well be maladaptive or
selectively neutral for another.
2. To understand the functional and evolutionary biology
plasticity, we may need to reassess the traits that we measure. Some
traits, perhaps unrecognized or unappreciated, may well be the foci
of the evolution of plant function, including adaptive plasticity.
Many traits we measure may be only artifacts or epiphenomena that
mislead our inquiry into the evolution of whole plant function.
Photosynthetic capacity and alternative measures of growth provide
3. Perhaps we should shift our discussion from plasticity
versatility -- not how a trait changes between environments, but
rather how a trait functions across its full range of potential
environments. Injudicious subsampling of the entire norm of reaction
may obscure the functional biology of plant responses to
These considerations touch on the limits
to interpretation of
adaptive plasticity in isolated traits in single species and suggest
the need for a broader view of functional linkages among traits in
species of known phylogenetic relationships.
The specialization hypothesis for phenotypic plasticity in plants
Christopher Lortie and Lonnie Aarssen, Department of Biology, Queen’s University, Kingston, Ontario, Canada.
Adaptive plasticity in plants is commonly interpreted for fitness estimates like size and fecundity. The specialization hypothesis however predicts that plasticity in such characters is not a product of selection, but rather, a product of specialized (i.e. ecotypic) adaptation to particular environmental conditions. In response to a recent test of this hypothesis (Emery et al. 1994), we refine its predictions to recognize that the evolution of specialized ecotypes may be accompanied by an increase, decrease or no change in the plasticity of size or fecundity. These predictions depend on whether specialization is associated with the less favourable or more favourable end of an environmental gradient, and on whether specialization to one end of the gradient comes at a cost of reduced performance at the other end. We argue that, for size or fecundity characters, a plastic response to environmental deterioration is adaptive only if the alternative is dormancy or death, and is generally less adaptive than phenotypic stability. Based on analysis of reaction norms for reciprocal transplants, we illustrate how it is possible to reject the specialization hypothesis and how to recognize results that are consistent with this hypothesis.
Plasticity of developmental hierarchies in plants
Ariel Novoplansky, Institute for Desert Research, Ben Gurion University, Sede-Boker Campus, Israel.
Allocation of resources
to newly developing organs depends on both the actual availability of the
limited resources and the probability that these organs will successfully
complete their life cycle. A central question is, what are the environmental
factors and the internal controls that govern the hierarchies and
sizes of newly developing organs.
Many plant organs are comprised of smaller functional units. For example, first-order branches would be functionally meaningless without their photosynthetic leaves. In this example there are two morphological hierarchies which are structurally and functionally nested within each other. Such hierarchical construction can be readily found in both the vegetative and the reproductive structures of most plants.
While allocation to relatively small organs allows swift materialization and low risk of invested resources, the development of relatively large organs allows greater efficiency in the vegetative or the reproductive expansion of the plant. The size of the developing organs thus represents an inherent trade-off between efficiency and risk in resource utilization. According to these considerations, it is expected that the determination of the hierarchy and the size of any given organ would not only depend on resource availability and the vigor of the plant but also on its evolutionary background (e.g. general probability of catastrophes), and on information concerning its specific environment (e.g. time left to the end of the season, probability of future competition, and probable future availability of limiting resources).
It is suggested that in addition to allowing plants their exceptional modularity, plasticity of developmental hierarchies allows plants better control over the efficiency and the risk of their developmental moves.
Scale limitations on phenotypic plasticity: some examples from plant foraging
Beàta Oborny, Department of Plant Taxonomy & Ecology, Lorand Eotvos University, Budapest, Hungary.
A common constraint
on plastic development is related to the time required for any developmental
move. If the environment is extremely variable compared to the time scale
of a plastic response, inducing signals often prove "misleading" by the
time at which products of the induced development materialize. In
such a case plasticity is not advantageous, because the environment does
not provide sufficient information about the future selecting conditions.
On the other hand, if the environment is relatively constant (i.e. phenotypic
change by induction is a rare event), the degree of selection may be insufficient
to favour plasticity over an
alternative rigid strategy. Therefore, we can expect that adaptation by plastic development is feasible only in a limited range of habitat types, where the temporal variation is intermediate.
If a plastic organism
is moving in space, temporal variation (on the scale of the response time)
interacts with spatial variation (on the scale of the distance travelled
during that time). In general, an important factor that determines the
of any plastic response is the quantitative match between the spatio-temporal patterns of the inductive and the selective factors in the environment.
As an example for measuring this match, I present a method from information statistics. This method directly enables the quantification of predictability of the environment.
Using Monte-Carlo simulations,
I studied the spatial dynamics of clonal populations in mosaic habitats
which consisted of resource-rich and poor patches. This system provided
examples for the degree of selection imposed on plastic behavior (in particular,
plastic rules of clonal growth) in environments which vary in space and
time. Using this method it was possible to demonstrate how different
spatio-temporal resolutions of
(b) morphological response,
(c) uptake of the resource
influenced the selective advantage of plasticity over rigid growth.
Multidimensional plastic responses of a clonal grass to light quality
Institute of Botany, Academy of Science of the
Czech Republic, Pruhonice, Czech Republic.
Red/far red (R/FR)
ratios are important environmental signals affecting both individual plant
behaviour and organization of whole communities. R/FR perception enables
individual plants to recognize their neighbours and forage for canopy gaps.
In grasslands, light patches are fine-grained. Since most of the grassland species are spreading clonally by means of stolones or rhizomes, the size of their ramets often exceeds the size of the light patches in their environment. Such plants are therefore expected to be highly sensitive to R/FR ratios.
In the current study I tested the spectral responsiveness of Festuca rubra which is one of the dominant species of the mountain grasslands of the Czech Republic. When exposed to lowered R/FR ratios, selected clones were found to differ in a) Number and size of tillers, b) Size and architecture of rhizomes, c) Size and architecture of roots. The fact that the below-ground organs responded to light quality implies shoot-root communication of unknown nature.
An independent study demonstrated that spatial patterns of above- and below-ground organs are at different scales. This finding indicates independent behaviour and plastic responses of shoots and roots although
such observation does not necessarily exclude the possibility of shoot-root
functional connection. This result is probably the outcome of interaction
of several environmental factors affecting above- and below-ground organs.
The study provides evidence for a rare interaction between signals perceived by the shoots and developmental responses of roots which could influence acquisition of soil resources.
Plasticity to light variation: a gateway to almost everything you were afraid to ask in evolutionary biology
Massimo Pigliucci and Hilary Callahan, Departments of Botany and of Ecology & Evolutionary Biology, University of Tennessee, Knoxville TN, USA.
The study of phenotypic
plasticity is moving from the backwaters to the
central stage of evolutionary biology, thanks to an intense empirical
and theoretical effort in the field during the last two decades.
Currently, more researchers are attempting to integrate evolutionary
biology, ecological genetics, and molecular developmental biology and
physiology to truly address the multifaceted and intrinsically
interdisciplinary field of phenotypic plasticity studies.
We discuss how research on plant plasticity to various aspects of light
variation (photoperiod, incidence, intensity, spectral quality) is
maturing to the point of allowing direct integration of previously
disparate fields of inquiry. Plasticity to light is being investigated
among species (comparative biology, macroevolution), among populations
of a single species (microevolution), or among genotypes within a
particular population (population genetics). Quantitative Trait Loci
mapping is making possible the study of variation in the genetic
architecture governing this plasticity in natural populations, while
mutant analyses allow for a dissection of the genetic machinery
underlying such architecture (functional genetics). Field research helps
in determining the type and intensity of selection acting on plasticity
to light, while phenotypic manipulations under controlled conditions
permit testing of adaptive hypotheses generated by field studies.
Finally, the fact that plants use a restricted number of photoreceptors
and transduction pathways to react to all sorts of light stimuli
presents the investigator with an excellent opportunity to study the
effects of costs and constraints on the evolution of plasticity to
different but related aspects of the environment.
Each of the points discussed here is illustrated with an appropriate
example from the research being conducted in our laboratory on the model
system Arabidopsis thaliana and its close relatives.
Developmental plasticity of the vegetative / reproductive balance
Tsvi Sachs, Department of Plant Sciences, The Hebrew University, Jerusalem, Israel
Vegetative and reproductive development are competing functions: they require
the same substrates and are mutually exclusive at the level of the individual
shoot apex. Yet many plants add both leaves and flowers at the same time. From
an adaptive point of view, this is presumably an expression of bet hedging in
unpredictable conditions (Amir and Cohen, 1990). It must also express
physiological mechanisms that determine the proportion, timing, and location of
individual events of apical conversion, from vegetative to reproductive
development. What could these mechanisms of apex allocation be, and how could
they facilitate and constrain the plasticity of the relations between the two
developmental alternatives (Sans and Masalles, 1994)?
The development of Senecio vernalis, a common ruderal plant in Israel, is a
prominent example of concomitant and plastic allocation to both vegetative and
reproductive functions. It germinates following the first rains, or in September
in irrigated locations, and may grow and bloom continuously from October to
April. Plants in close proximity are stressed by compacted soil, shallow
substrate or shade, are vigorous in disturbed, unoccupied locations, or are
"controls" growing in conditions undistinguished in any obvious way. Size
parameters of such neighboring plants could readily differ by factors of many
The first capitula opened before branches developed, always at the tip of the
original, embryonic axis. The only parameter correlated with this apical
conversion was the number, about 15, of nodes (and leaves). Plants growing in
different times and conditions excluded any effect of a critical photoperiod.
Though there were somewhat fewer nodes along the first axis in small, presumably
stressed, plants, this could not account for the very large differences in plant
size. These differences were due primarily to the sizes, rather than numbers, of
the various organs, including the reproductive capitula. A major contribution
was made by the size of the leaves, which differed primarily in the number
rather than dimensions of their cells.
The top two or three branches developed in all but the most stressed plants,
and their role was primarily reproductive. Here, too, node counting was evident:
the flowering lateral apices completed the number of nodes separating them from
the roots to the number characteristic of the plant. Thus the top branch formed
an inflorescence directly, while the second formed one small leaf whose
auxiliary bud could form another inflorescence, etc. The number of capitula
carried by the leaves on the original axis could thus vary, and this could
extend the time during which the same leaves supported the reproductive effort.
It was the lower branches that expressed the greatest plasticity, in their
occurrence, vigor and in the number of leaves they carried before reproductive
development. In plants that branched but were not very vigorous the higher the
location of the branch the fewer the leaves it formed before becoming
reproductive. The total number of nodes separating the capitula from the roots
was more or less constant, and similar to that formed on the main plant axis.
Flowering did not occur on branches with fewer nodes. The situation in vigorous
plants was different. Each of the lateral branches could carry more leaves, up
to starting its own "node counting", forming as many nodes as the original axis.
Large deviations from this number were not found; vegetative growth could be
continued on secondary lateral branches, and these, again, did not form more
than the characteristic number of nodes and leaves. The result of repeated
branching was a candelabra of yellow capitula.
The effects of stress on "node counting" were confirmed by laboratory
experiments with early blooming Pisum sativum cv Alaska. The number of nodes
formed was remarkably uniform, even in plants with different leaf sizes kept
under varied environmental conditions. Stress conditions (the removal of large
parts of the cotyledons) reduced leaf size but had at best a small effect on the
number of nodes formed before the initiation of the first flower primordia.
These observations require mechanisms that are more sophisticated than source /
sink relations: substrates, by definition, are essential for all types of
development, and their availability could not be expected to determine its
nature. An important component of the allocation of development to vegetative
and reproductive functions is related to size, but it is not overall size that
is critical but rather the developmental past of individual apices, which is
expressed by the number of nodes they have formed. Evidence for what might well
be the same mechanism of "node counting" is available in both the physiological
and agricultural literature (Sachs, 1991), and in maize and tomato there have
been analyses of its variation in response to single gene changes. The present
report, however, appears to be the first to point out its ecological
implications and its relation to developmental plasticity.
One advantage of a mechanism of "node counting" may be that it does not act at the level of the entire plant. It thus allows for both vegetative and
reproductive development to occur concurrently. It also means that decisions
about apical conversion are gradual, and may be based on cumulative information
(Sachs, 1991). Further, "node counting" provides for the formation of units,
presumably of adaptive significance, that include both vegetative and
reproductive structures. It is a mechanism that constrains but does not preclude
plasticity. One reason is that the number of nodes does not determine the size
of the functional units: the sizes of both leaves and capitula vary greatly, and
even the number of capitula formed at the tip of any given axis can be
modulated. Another source of plasticity is that the counting mechanism itself is
plastic - but only within relatively narrow limits, the largest differences
being between completing the required number of nodes separating an apex from
the roots and a "rejuvenation" of the counting device.
The choice between vegetative and reproductive development at the level of
individual apices is a prime example of non-cognitive behavior. It extends our
earlier suggestion (Sachs et al. 1993), that choices between the development of
alternative organs of an individual plant (different branches, different roots)
are central expressions of phenotypic plasticity.
Amir, S. and
Cohen, D. 1990. J. theor. Biol. 147, 17-42.
Sachs, T., Novoplansky, A. and Cohen, D. 1993. Pl. Cell Env. 16, 765-770.
Sachs, T. 1991. Pattern Formation in Plant Tissues. Cambridge University Press,
Sans, F. X. and Masalles, R. M. 1994. Can. J. Bot. 72, 10-1.
Plasticity integration: Coordinating the phenotype across changing environments
Carl D. Schlichting, Department of Ecology and Evolutionary
University of Connecticut, USA.
The nature of how phenotypic characteristics are integrated
is of fundamental interest to evolutionary biologists, and increasing effort
has been invested in examining this issue using organisms that develop
in relatively constant environments. Little attention, however, has been
focused on how this is accomplished when the organism, depending upon conditions,
‘chooses’ among multiple developmental pathways.
In the workshop, I will take the following approach. First, we will step back and ask what the fundamental issues are, taking a mechanistic, developmental perspective. Second, I will briefly discuss the conceptual approaches taken to examining integration, most notably genotype-phenotype mapping and quantitative genetics, and point out their pros and cons. Finally we will look at some actual data sets derived from plasticity studies to examine questions relating to both the inputs and outputs of studies to examine plasticity integration.
Controls and limits of plasticity
Bernhard Schmid and Diethart Matthies, Institut fur Umweltwissenschaften der Universitat Zurich, Switzerland.
Because plants can
grow and branch continuously they show much phenotypic
plasticity. Nevertheless, several plant structures such as leaves, flowers, and
especially fruits have a more determinate development, size, and shape. At the
beginning of ontogenetic development, plasticity may be limited by the genetic
program (architectural blueprint), whereas later on the environment largely
controls phenotypic variation. This variation is narrowed again as the degrees
of freedom are reduced by the ontogenetic development itself, e.g. due to
allometric constraints or when plants change from vegetative growth to sexual
reproduction. To illustrate these points the early development of native clones
of Solidago altissima was followed in the field and the phenotypic variation of
seedlings and cuttings of these plants was measured in contrasting environments
in the experimental garden. Further, plants of the annual Thlaspi arvense were
exposed to light and/or nutrient pulses either early, at an intermediate time,
or late during development and their reproductive allocation (number of flowers,
number and size of seeds) was analyzed. Controls and limits of plasticity in
plants can only be disentangled by experimental approaches. The analysis of the
mechanisms, however, does not yet address questions of their adaptive
The adaptive evolution of plasticity in natural populations: benefits and costs of shade avoidance responses
Johanna Schmitt, Susan Dudley1, and Kathleen Donohue, Department of Ecology and Evolutionary Biology, Brown University, Providence RI, USA.
1 Present address: Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada.
We are using shade avoidance responses in the North American annual Impatiens capensis as a model system for investigating the adaptive evolution of phenotypic plasticity. Natural populations of this species occur in sites ranging from forest understories to full sun, and seedling densities are highly variable, ranging up to 3000/m2. Plants exhibit dramatic phytochrome-mediated stem elongation and other shade avoidance traits in response to intraspecific competition. Selection on these traits is density dependent. Plants expressing the shade avoidance response have high relative fitness in dense stands due to direct selection on height, but low relative fitness at low density due to some intrinsic cost of the shade avoidance phenotype unrelated to height. Greenhouse experiments have revealed significant within-population genetic variation in responses to density and R:FR, suggesting the potential for reaction norms to evolve in response to such selection. We have also observed ecotypic differentiation in shade avoidance responses on a fine spatial scale between populations from open and woodland. Genotypes originating from an open site, where R:FR is a reliable cue of neighbor competition, are less responsive to simulated foliage shade than genotypes from woodland sites, where R:FR is lowered by the forest canopy.
To test the hypothesis that this population differentiation is adaptive, we performed a reciprocal transplant experiment in which inbred families from an open and woodland population were planted into both sites in both high and low density. We could thus measure plasticity of shade avoidance traits and fitness to density and to site characteristics (such as overhead canopy) independent of density. We will report the results of phenotypic selection analyses to test the hypothesis that local adaptation is attributable to direct, site-specific selection on shade avoidance traits. Genotypic selection analysis will allow us to examine selection on family reaction norms in each site, and to test the hypothesis that there is a maintenance cost to this form of plasticity.
Building upon "A framework for plant behaviour"
Department of Biology, The Open University,
Milton Keynes, UK.
Nearly ten years ago Deborah Gordon and I proposed that the behavioural repertoire of plants could be neatly encapsulated by a two-dimensional classification based upon plants' sensibilities to different kinds of stimuli and their
capabilities to respond to them (Annu. Rev. Ecol. Syst. (1989) 20: 349-366).
In this paper I review the last ten year's progress in the exploration of
plant behaviour and ask whether the proposed framework is still useful and
illuminating. The emphasis in our earlier paper was on how modularity permits
plants to alter their structure in response to changes in the environment,
providing plants with a mechanism equivalent to the behaviour of unitary
animals. While this is undoubtedly the most important behavioural mechanism in
plants because it is so general, many plants are also capable of moving their
flowers, stems or leaves in response to environmental stimuli. We now consider
the phylogenetic distribution of the capability of movement in relation to
The phytochromes – plurality in perception, flexibility in function
Harry Smith, Department of Biology, University of Leicester, LE1 7RH, UK.
Plants exhibit a high degree of plasticity in their responses to signals from the light environment. The perception of light signals is mediated via photoreceptors, and the phytochromes are the best characterised of all plant signal-transducing photoreceptors. The phytochromes exemplify, par excellence, the concept that functional plasticity depends upon pluralistic perception mechanisms and flexible response systems. Based upon the current fixation for Arabidopsis as the role model, the phytochromes are encoded by a diverse family of five PHY genes, PHYA, B, C, D and E. Surveys of a large number of angiosperm families indicate that PHY gene families similar to that of Arabidopsis are present in most, probably all, flowering plants (Matthews et al, 1995). Within Arabidopsis, the phytochromes share some highly conserved domains, including those involved in chromophore binding and in dimerisation, but there are also highly divergent regions. The apoproteins of phyB and phyD are more similar to each other (ca 80% amino acid identity) than they are to phyA or phyC (ca 50% identity), whilst phyE is somewhat closer to phyB and phyD than it is to phyA and phyC. The picture, therefore, is of a family that has diverged substantially throughout evolution, but which retains highly conserved elements crucial to function.
The functions of the phytochromes may be conceptually regarded as being two-fold; they detect light stimuli and they evoke specific responses. In other words, each phytochrome has both a sensory and a regulatory function, and it is logical to propose that the two functions reside in different portions of the molecule (Quail et al, 1995). As far as is known, all the phytochromes bind an identical chromophore (a linear tetrapyrrole that absorbs maximally in the red and far-red spectral regions) so that each phytochrome is presumably capable of detecting signals of red and far-red radiation. The regulatory functions are, however, different and considerable effort has been expended recently to identify the physiological functions of each phytochrome in Arabidopsis. The view is emerging that the phytochromes use common light signals to evoke varying responses that are individually important at different stages of development (see Smith, 1995 for review). The existence of multiple photoreceptors allows a flexibility of response that could be described as plasticity. Because there may be overlap, co-operation and even conflict between the roles of the different phytochromes, the outcome of specific signal-response events may not be readily predictable; in other words complexity leads to unpredictability. Unpredictability seems to be the principal characteristic of what we like to call plasticity.
The most powerful approach to identifying the functions of individual phytochromes is through the selection of mutants. In Leicester, we now have lines of Arabidopsis that have genetic lesions in each of the PHYA, B, C, D, and E genes. Surprisingly, only the phyB mutant shows a marked phenotype at the mature plant stage. This means that the lack of individual phytochromes does not necessarily spell disaster. Indeed, the original phyD mutant was the natural ecotype Wassilewskija, or WS, which has been shown by Aukerman et al. (1997) to have a large lesion in the phyD gene, although it survives quite successfully in its own natural habitat. Does this mean that phyD is superfluous? In a sense this may be so, in the same way that to be colour-blind or tone-deaf does not necessarily mean that success in life is impossible, although being so afflicted one would be unwise to try to emulate Michelangelo or Beethoven. The Arabidopsis phytochrome mutants are ecologically disabled, in the sense that the loss of an individual photoreceptor limits the range of environmental light signals to which the plant can successfully respond. Plurality of perception provides flexibility of function.
The plurality resides in the gene family. In theory, gene families provide a mechanism for generating plurality that is, from the evolutionary viewpoint, both economical and secure (Smith, 1990). Gene duplication, unequal recombination, domain swapping and mutation collectively provide a mechanism for parsimonious and safe evolutionary experimentation, and we can have no idea how many variants of important genes, such as the phytochromes, have been tried out and discarded through evolution. Teleology apart, the testing of variants within the framework of a gene family is just one example of the benefits of complexity. For the phytochromes, continual refinement of photoregulatory perception through the generation of phytochrome variants capable of evoking new transduction pathways has led to the present pluralistic state in which the various phytochromes are capable of regulating all phases of development from germination to flowering.
The phytochromes are a simple family of small size, but they may be regarded
as a paradigm of functional plasticity. Gene families are the
rule, rather than the exception, in all higher organisms, and it seems
inescapable that one of the benefits of the evolution of gene families
is the plasticity that they endow.
Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Amasino RM, Sharrock RA (1997) A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 9: 1317-1326
Matthews S, Lavin M, Sharrock RA (1995) Evolution of the phytochrome gene family and its utility for phylogenetic analysis of angiosperms. Ann. Missouri Bot. Garden 82: 296-321
Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochrome photosensory perception and signal transduction. Science 268: 675-680
Smith H (1995) Physiological and ecological function within the phytochrome family. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 289-315
the interplay between environmental predictability & phenotypic plasticity
in stoloniferous and erect herbs
1Josef F. Stuefer, 2M. Esther Perez Corona and 1Heidrun Huber,
1Department of Plant Ecology & Evolutionary Biology, Utrecht University, The Netherlands,
2Departamento de Ecologia, Universidad Complutense de Madrid, Espana.
From an evolutionary
point of view, phenotypic plasticity can be seen as a
functional response of plants to predictable unpredictability in
environmental conditions. Plasticity is a trait which enables plants to
respond to unpredicted changes that arise during their life cycles. In
order to create selection pressures for phenotypic plasticity, however,
such unpredictable changes in the environment of species need to occur at a
certain frequency and with high predictability over evolutionary periods
Patterns of internode and petiole plasticity in erect and in
stoloniferous herbs provide circumstantial evidence for this notion.
Shade-induced changes in their length correlate with patterns of long-term
predictability in light supply in their native habitats. Vertically
oriented spacers of herbaceous plants (i.e. petioles of stoloniferous,
internodes of erect species) show consistently higher degrees of plasticity
in their length than horizontally oriented spacers do. This pattern seems
to be generally valid for a broad range of species. It is suggested that
phenotypic plasticity in the length of vertical structures is favoured
during evolution, because it yields predictable benefits in terms of
enhanced light capture in most herbaceous canopies where light conditions
improve steadily with increasing distance from the soil surface. Elongation
of horizontal spacers, on the other hand, seem less likely to result in
reliable benefits for a plant, as patterns of light distribution in the
horizontal plane are usually less predictable than vertical light
Field data from natural habitats of stoloniferous species such as
Potentilla anserina have been collected to quantify spatial patterns of
light supply in the horizontal and in the vertical plane. These data can
also be used to calculate measures of predictability on spatial scales
relevant to clonal and erect plants native to this system. Random line
transects of 10m each have been laid out in a dune grassland, and light
availabilities were meausred by the use of digitalized vegetation images,
calibrated for relative light intensities. These data show that levels of
spatial predictability in light supply are considerably higher in a
vertical than horizontal direction. They thus support the notion that
differential degrees of phenotypic plasticity in the length of vertically
and horizontally oriented spacers may ultimately be related to
environmental predictability in resource supply patterns.
effect of plastic storage allocation on the size hierarchy in a populati
on of a perennial plant under variable environmental heterogeneity
Suzuki & 2Takuya Kubo
1The Institute of Low Temperature Science, Hokkaido University, Sapporo, Japan, and 2Department of Biology, Kyushu University, Fukuoka, Japan.
Perennial and annual
plants often differ in their allocation to reproduction. While annuals
usually allocate most of their assimilates into vegetative growth and switch
to reproduction at a later developmental stage, most perennial plants store
some proportion of their resources concurrently with their aerial shoot
development. This allocation into storage may affect the competition ability
of the shoots and consequently the size hierarchy of the plants.
We would like to present a simulation model of a shoot growth of a perennial plant in which each shoot consists of a productive part including stems, leaves and a storage organ such as a rhizome or a tuber. Each shoot photosynthesizes and can allocate its assimilate to either parts, but movement of resources among shoots is not allowed. Shoots compete asymmetrically with their neighbours. We considered two cases; (i) allocation of assimilates to storage within a shoot is genetically determined, and (ii) allocation could be altered in a plastic manner, depending on the shoot's surrounding environment. Comparing shoot growth in the two cases under homogeneous and heterogeneous environments, we got the following: (i) Under environmental homogeneity, there were no significant differences between the deterministic and the plastic plants in a mean shoot size and a size hierarchy of the shoot population (ii) Under some heterogeneous conditions, the plastic plant had some advantage over the deterministic one. These results suggest that environmental heterogeneity favours plastic response of resource allocation in a perennial plant.
and morphological variation in white
clover in response to a heterogeneous light environment
Roy Turkington and Clive Welham, Botany Department, University of British
Trifolium repens (white clover) is a common species in pastures throughout the temperate region. It's ability to persist in pastures is largely attributed to its capacity for clonal growth via the lateral spread of stolons. White clover exhibits a guerrilla strategy, a growth form characterized by prostrate growth, rapid stolon elongation and relatively infrequent branching. Each stolon is comprised of numerous ramets (each ramet defined as a node with its associated internode, leaf, and axillary bud) and stolon elongation is a consequence of ramet proliferation. A given stolon can grow longer than 25 cm before fragmentation occurs thereby giving rise to numerous individual ramets, each capable of independent existence. This growth form, combined with the fact that an individual clone (genet) can be long-lived, results in ramets being distributed widely across the pasture.
As a clover grows through a pasture it encounters a complex canopy structure. Besides intermittent penetration of sunlight through spaces between leaves, there may be larger gaps that allow penetration of sunlight for longer duration. These larger sunflecks can supply a substantial portion of the energy for a plant's photosynthesis. A plant within a sunfleck will also receive light from the clear sky that has been transmitted through leaves and in many cases, light that has been reflected off plants forming the boundary of the sunfleck. The relative proportions of transmitted, reflected, and unfiltered light will be influenced by biotic (location, identity, and conditions of neighboring vegetation) and abiotic (diurnal and seasonal solar movement, cloud cover) factors. Therefore, the light climate itself can differ in terms of the total light available (light quantity) and/or its spectral composition (light quality). Arguably, one of the main characteristics conferring success on an individual is phenotypic plasticity, the ability to make morphological and physiological adjustments to changes in the environment. To continue growth and gathering of resources, the plant may need to modify its phenotype as it continually encounters the patchiness in its environment.
By manipulating the light environment under controlled greenhouse conditions, there is considerable evidence to demonstrate how light quantity and quality affects plant growth and morphology. In many studies, however, shading of target plants is typically accomplished artificially (using synthetic material) and abruptly, and the treatment is usually imposed for longer than the normal diurnal period. This is in contrast to the natural environment where the quality and quantity of light will vary gradually and continuously in space and time. If a plant's behavior is dependent upon the degree of resource depletion, then imposing a sudden depleted condition might evoke responses quite different from those normally exhibited in the field. Whether the standard protocol in light experiments constitutes a reasonable approximation to the natural condition is unknown.
Here we report the phenotypic response of white clover to heterogeneous light conditions. In the first experiment, patches of reduced light were imposed artificially and abruptly upon two consecutive ramets (termed first and second ramets) on a stolon. First ramets were either shaded or unshaded, whereas all second ramets were shaded. In a second experiment, neighboring grasses were used to shade basal and/or apical regions of stolons and their effect upon apical growth and morphology determined. A third experiment examined the effect of patchiness due to shading by grasses, and of light reflected from grasses on the growth and morphology of white clover.
Long-term exposure to artificial shading (Experiment 1) had no effect upon rooting, branching, or flowering frequencies of first ramets, when compared to the unshaded treatment. However, shaded first ramets had significantly smaller leaf areas, internode lengths, and root and shoot masses, than control ramets, whereas petioles were significantly longer. Second (shaded) ramets had significantly smaller leaf areas and shoot masses when the first ramet was also shaded suggesting an integrated response between ramets.
Using the more natural or more realistic treatments (Experiments 2 and 3) produced effects that were more subtle. In experiment 2, shading of the apical region produced no significant change in apical morphology when basal regions of the stolon were either shaded or unshaded. When the apical region was unshaded, however, the light environment in the basal region resulted in significantly reduced branching propensity and total ramet production in the apical region. Shading of the entire stolon (experiment 3) caused a significant reduction in branching propensity, total stolon length, ramet production, leaf area, and shoot mass. Petiole and internode lengths were unaffected by the presence of grasses. There were no significant changes in stolon morphology for reflected versus unshaded treatments.
Taken together, these results suggest that (1) severe and abrupt interference of the light environment (experiment 1) can induce significant changes in the growth and morphology of clover stolons, (2) these changes are reduced (or non-existent) when available light is manipulated to create more "natural" conditions, and (3) to determine the ecological implications of this phenotypic plasticity, it will be necessary to obtain an accurate profile in the field of the typical light environment .
Fernando Valladares1, S. Joseph Wright2 and Robert W. Pearcy3
de Ciencias Medioambientales, CSIC, Madrid, Spain,
2Smithsonian Tropical Research Institute, Panama,
3University of California, Davis, USA.
In any given region, it is possible to separate co-occurring species that have similar roles and effects on ecosystem processes into functional groups. While in certain poor habitats each species is functionally unique, in complex ecosystems like tropical rainforests species overlap in function. Comparative ecology typically considers mean performance of the species compared, and frequently fails to find mechanistic differences among the species. Since habitat conditions are constantly changing, plastic response to environmental variability can be as important as overall performance. We studied phenotypic plasticity in response to light in 16 shrubs species of the genus Psychotria co-occuring in the understory of a tropical rainforest, in order to explore its contribution to the understanding of species function in hyperdiverse environments. Six species were more frequent in forest gaps and the other ten were typically found in the dark understory. Several individuals of each species were grown in three light environments designed to give similar daily photon flux densities to the natural light gradient observed in the forest of Barro Colorado Island (Panama). Average values in each light treatment and plastic response expressed across light treatments were determined for several structural, physiological and growth parameters. When individuals grown under the same conditions were compared, plant performance and mean values for most structural and physiological parameters studied were remarkably similar among the 16 congeneric species. In contrast, species significantly differed in their plastic response to the light treatment. Species that exhibited in the field a preference for brighter environments (small forest gaps) exhibited a higher mean phenotypic plasticity than species frequently found in the darkest areas of the forest understory. We suggest that not only differences in the heterogeneity of the light environment but also on the predictability of the environmental change (gaps always tend to close while gap formation by treefalls is unpredictable) are responsible for the observed differences in phenotypic plasticity. And these differences might have more dramatic implications for survival and might be more ecologically relevant than differences in species performance in a given environment. Phenotypic plasticity seems to be a valuable feature for understanding the different ecological roles in complex habitats of sympatric species that are apparently redundant from a functional point of view.
Genetic and environmental effects on character correlations under selection
Peter H. van Tienderen and Arjen van Hinsberg, Netherlands Institute of Ecology, Centre for Terrestrial Ecology, Heteren, The Netherlands.
Several authors have
argued that observed correlations among different
characters appear to facilitate concerted responses to selection, labelling
them synergistic, reinforcing, or protagonistic. In Plantago lanceolata,
plants with long leaves also form large spikes with heavy seeds, traits that
are beneficial under shady conditions. Furthermore, artificial selection on
leaf length under simulated shade not only increased survival and
reproduction in the shade, it also reduced germination under conditions not
suitable for growth and establishment. Such favourable correlations can not
readily be explained by individual selection, at least not in a panmictic
population. A correlation is a characteristic of a population rather than an
individual. Directional selection will deplete favourable (co-)variation,
and antagonistic pleiotropy will retard further evolution. Thus, one would
expect unfavourable rather than favourable correlations.
Therefore, we need to think about scenarios that can explain the
evolution and maintenance of favourable correlation structures, what some
would call 'architecture'. The following possibilities are discussed:
1. Populations with favourable correlations can track temporal changes in
2. Specific adaptive landscapes give rise to favourable trait associations,
as a result of the balance between selection/mutation/drift.
3. Correlations are side effects of underlying developmental processes,
sometimes advantageous, sometimes not.
4. Correlation structures are the indirect results of selection for
Succulence: How to combine business with pleasure?
Yoav Waisel, Department of Plant Sciences, Tel-Aviv University, Israel.
Salt induced succulence is usually described by two traits: by increased size of leaf cells and by an increase in the leaf water content. Succulent plants have several common features: they have thick leaves, large mesophyll cells, small intercellular spaces in the leaves, higher elasticity of the cell walls, highly developed water storing tissues, a relatively small ratio of the outer leaf surface area/leaf volume, lower content of chlorphyll per unit volume and a lower density of the stomata.
What causes succulence?
Several answers were given to that question.
a) Succulence represents a direct response of the plant to a high content of NaCl.
b) Succulence results from accumulation of organic acids.
c) Succulence develops due to changes in the ionic balance of the leaf cells.
d) Succulence development is correlated with an increase in ATP content, induced by an inward sodium transport.
e) Succulence is induced by the effects of chloride. Chloride loosens some binding complexes in the walls, and by that enables their expansion and eventually the increase in size of the mesophyll cells.
Neither one of the above hypotheses gives a full answer and an alternative suggestion will be presented.
Selection pressures and the phenotypic plasticity of plant defences
David Ward, Mitrani
Center for Desert Ecology, Blauestin Institute for Desert Research, Ben
Gurion University of the Negev, Sede Boqer Campus, 84990
Inducible defences against herbivory constitute a form of phenotypic plasticity. Inducible defences are likely to evolve only under those conditions where maintenance of these defences under conditions of low herbivory constitute a significant cost for the plant and where the defence can be produced sufficiently quickly that they can either deter either the current herbivores or at least deter future herbivores, if the current level of herbivory is a reliable indicator of future herbivory. Among a number of general hypotheses of plant defence, the resource availability hypothesis (Coley et al. 1985) and variants thereof is most prominent. This hypothesis states that plants growing in environments with low resource availability should invest in defence at the expense of growth because the cost of replacement of a part that is eaten is high. Conversely, plants growing in resource-rich environments can easily replace a part that is eaten and thus should invest in growth at the expense of defence. This hypothesis explicitly states that plasticity of defence is contingent upon the abiotic environmental context in which the plant is found, and implies that the level of herbivory suffered by the plant is relatively unimportant in determining the degree of defence employed. Similarly, no mention is made of the role of phylogenetic factors in determining the type and level of defence employed. Yet both level of herbivory and phylogeny have been shown to affect defence production. I examine the physical (e.g. thorns) and chemical (e.g. tannins and calcium oxalate) defences of a number of plant species growing in resource-poor environments in Africa and the Middle East in the light of the resource availability hypothesis and competing hypotheses, and compare these results with those obtained from more mesic environments in order to ascertain whether abiotic environmental factors are indeed of primary importance in the plasticity of plant defences.
Developmental phenology and the timing of determination of shoot bud fates (clonal and non-clonal considerations).
A. Watson, 2Cynthia S. Jonesand and 3Monica A. Geber,
1Department of Biology, Indiana University, Bloomington, Indiana,
2Department of Ecolofy and Evolutionary Biology, University of Conneticut, Storrs, CT, USA.
3Section of Ecology and Systematics, Cornell University, Ithaca, NY, USA.
Plasticity is one of
the essential features of plant adaptation. It results from the fact
that plant growth is modular, which allows alteration in the number, size
and function of modules made at different times and at different stages
in plants's life histories. To an important degree, the extent of
plasticity expressed is a function of the interaction between plants' developmental
patterns and patterns of environmental variability.
The pattern and timing of meristem production, longevity and commitment,
and the likelihood that meristems at different locations and of different
ages respond to the environment in particular ways -- causing them to
experience different developmental fates -- can be thought of as traits, or
suites of traits, that together comprise the plant's developmental program.
Thus, to understand the role of developmental pattern in adaptation it is
important to understand what regulates the production and differentiation
of meristems. Our goal here is to explore developmental and environmental
constraints on the timing and pattern of meristem determination, and the
role these constraints play in modulating the expression of plant
to be cynical, when to be gullible: cue reliability and optimal
Theodore G. Wong, Department of Biological Sciences, Stanford University, Stanford CA, USA.
responses to inappropriate environmental cues may
comprise a major fitness cost of phenotypic plasticity. Cue unreliability
results when in a multidimensional environment, the values of perceived
environmental cues do not covary perfectly with the values of
physiologically important environmental variables. I present a model of
optimal biomass allocation to vegetative and reproductive growth which
includes explicit treatment of the information content of environmental
cues. The plant is represented as an optimal translator, whose input is
the sequence of cues and whose output is the fecundity schedule. Both
the entropy of the fecundity schedule (and hence the gradedness of
reproductive allocation) and the fitness cost of plasticity depend
directly on the reliability of environmental information. Given
unreliable cues, the successful plant adopts a fixed, bet-hedging strategy
rather than a plastic, specialized strategy. I discuss implications of
the model results for the evolution of phenotypic plasticity and for
physiological responses to climate change.