Gulsum Soyler-Ogretim

Gen 535

04.27.04

 

FINAL DRAFT "PHENOTYPIC PLASTICITY"

 

I. Introduction:

 

Phenotypic plasticity is the capability of a genotype to show different phenotypes depending on environmental conditions. It is the area of interest for important biological disciplines such as evolution, ecology, and molecular biology. Almost all kinds of organisms including microorganisms, plants, and animals show plasticity. Plasticity in Daphnia is the very first example studied by Woltereck (1909). Daphnia normally produces helmet against its predators, but it is possible to make Daphnia to produce helmet even if there is no predator, since some chemical compounds are the ones triggering helmet production.

 

In 1911 Johannsen made separation clear between genotype and phenotype. He found that even a homozygote line could show variation and his explanation was on the possibility of being non-genetic factor that is environment affecting this variation. In 1949 a Russian scientist Schmalhausen made important explanations on evolution of plasticity. He showed clearly the external and internal factor differences in the origin of change and seemed both to be equal. He also introduced reaction norm. Reaction norms shown as straight lines are described as the relationship between environment, phenotype, and genotype. Slope displays the plasticity. Reaction norm and plasticity are not the same. Whether a genotype has plasticity or not does not affect itŐs having reaction norm. To be able to draw reaction norm graph, the results of analysis of variance (ANOVA) is needed. If there is no plasticity, the reaction norm is parallel to the environmental axis. If there is no variation for plasticity, reaction norms are parallel to each other.

 

In 1965 Bradshaw made a review called "evolutionary significance of phenotypic plasticity in plants". He saw the interaction between genes and environmental effects very complex. He said that there is relationship between the rapidity of development and the degree of affection by environment. According to him, if plasticity has genetic variation, it should have its own genetic control. In 1974, Lewontin criticized a study on IQ in humans. He said analysis of variance is not the same as analysis of cause and added that heritabilities could change in response to different environments.

In 1985, Via and Lande studied on microevolution of phenotypic plasticity. They said that a reaction norm is the same as genetic correlation for the same traits in different environments. They presented restrictions for the evolution of reaction norms. Standardized genetic covariance between two traits gives genetic correlation. It is an alternative method to reaction norm analysis. It can be calculated. Pleiotropy and linkage cause positive or negative genetic correlation. According to this approach, plasticity is the result of selection, not the aim of selection.

 

The relationship between genotype and phenotype is called as genotype-phenotype mapping function (G-P). Simple G-P mapping function at molecular level explains that one gene generally encodes one protein. As for quantitative genetic mapping function, one gene can affect multiple characters at the same time (pleiotrophy) or genes affect the functions of other genes (epistasis). Further, environment is also important factor affecting genes to produce different phenotypes. The last and more complex model is about the effect of development on interaction between genes and environment (epigenetics).

 

One of the most comprehensive books written about plasticity is "Phenotypic Plasticity-Beyond Nature and Nurture (Pigliucci 2001)". Pigliucci covers this subject from nearly every aspect. His contribution to better understand the plasticity also helped to the preparation of this paper.

 

After given basic concepts and brief historical background of phenotypic plasticity, the rest of the paper will continue to explain the methods to study plasticity, genetics, molecular biology, and ecological significance, evolution of plasticity as well as developmental and behavioral plasticity. C

 

II. How to study phenotypic plasticity:
 

To study how and why plasticity occurs, experimenters use a number of experimental methods. 
Statistically, complete factorial design, split plot, or Latin square designs are the ones mostly used. 
Since plasticity means to change phenotype in response to distinct environments, researchers treat the 
organisms with biotic or abiotic environmental factors such as different conditions of temperature and 
food for animals and of water, light and nutrients for plants. Considering variation with multiple 
genotypes from different populations' different species, plasticity studies are difficult to carry 
out needed a lot of blocking. After analyzing the results with analysis of variance or genetic 
correlations statistically, they are presented as reaction norms or environment-environment plots.



Transplant experiments are other way to study plasticity either in green house or in lab. These experiments interested in adaptive
 phenotypic plasticity originate from ecotype studies dealing with specialized species adapted to a narrow specialized environment to survive such as alpine plants. 
The goal of these experiments is to pick several genotypes from multiple locations, clone them and locate back into different locations. 
Even though transplant examples are useful to see the effects of multiple environments, it is hard to interpret the causes of phenotypic variation.


Another approach to study genetics and evolution of phenotypic plasticity is phenotypic manipulation. The basic idea here is to trick the 
organism to show the plastic response without appropriate conditions. For example helmet production in the absence of predator or 
shade avoidance plasticity in Impatiens capensis 
without vegetation shade. Another way of testing plasticity by manipulation is to prevent plastic response by single gene
mutation. By doing this, some important information about the genes responsible for plastic response can be gathered.
 
Artificial selection is also a method to change population mean by selection and to show that plasticity is genetically affected. There are studies with Nicotiana rustica
and Drosophila melanogaster
. QTL (quantitative trait loci) mapping technique also studies the genetics of plasticity. RFLPs (restriction fragment length polymorphism) or RAPDs (randomly amplified polymorphic DNAs) and AFLPs (amplified fragment length polymorphisms) are used to find the localization of QTLs. It is very old and accurate to find out the gene of interest.
style='font-size:12.0pt;font-family:"Times New Roman"'> 
III. Genetics of phenotypic plasticity:
 

Are there plasticity genes? This is the most suitable question for discussion in plasticity studies. Via (1993) does not accept that there are separate plasticity genes. Instead, she explains phenotypic plasticity as differential allelic expression whereas Scheiner and Lyman (1991) describe it as a trait itself (Jong 1995). Schlichting and Pigliucci (1993) also investigated the genetic control of phenotypic plasticity. They said that plasticity probably controlled by multiple loci. They disagreed with Via (1993) at some points and said that there are plasticity genes as regulatory loci. Pigliucci (2001) agrees with Scheiner and Lyman and adds that because reaction norm is related to genotype, plasticity must be under genetic control.

 

Scheiner and Lyman (1991) suggest three possible models for the genetic bases of plastic responses:

1. Overdominance: Homozygosity increases the plasticity.
2. Pleiotropy: Like pleiotropic gene effects, plasticity is the response of the same group of alleles to different environments.
3. Epistasis: Reaction norm (plasticity and height) is under the control of 2 groups of genes.
 
There are 3 different variation types for plasticity: within-population, among-population and among-species. As an example for variation within-population, the study of Brakefield and French (1999) can be given. They showed seasonal polyphenism on the eyespots of butterfly wings. Cook and Johnson (1968) studied the ability to produce two or more types of leaves within and among 10 populations of Ranunculus flammula and observed variation-among population. As for variation within-species, Mitchell (1976) studied nine species of Polygonum to look at submergence and found variations.  
 
Besides genetically, plastic response can also be obtained maternally. Agrawal et al. (1999) studied maternally induced transgenerational induction in Raphanus raphanistrum and Daphnia cucullata. Their results showed that when a plant is exposed to a herbivor or an animal is exposed to a carnivor, it causes the organism to produce defend for it and better defended offspring. 
 
 
 
 
IV. Molecular Biology of phenotypic plasticity:
               
There are a number of studies for the molecular biology of plastic responses, yet need to be named as plasticity. QTL studies provide important data for molecular biology of plasticity. Researchers analyze F2 and F3 individuals for QTL mapping. 
 
Based on QTL mapping studies, Pigliucci (1996a) describes plasticity genes as "regulatory loci that directly respond to a specific environmental stimulus by triggering a specific series of morphogenic changes". However, not all regulatory genes are plasticity genes. Plasticity genes are environment specific. They work together with other genes affecting phenotype and are really crucial for the evolution of adaptive plasticity
 
There are three types of plastic response to environment: 
"1. Specific responses elicited by one particular type of stress 
2. Responses induced by a limited number of stresses
3. Generalized responses to a variety of stressful situations" (Pigliucci 2001)
Heat shock response is a classical example for specific response (Wu et al. 1994). In this response special proteins are produced to prevent denaturation of other proteins by high temperature. 
 
Plasticity genes encode the receptors to response environmental effect, usually triggered by hormones, for example, genes for photoreceptors in plant and animals, and many bacterial genes. Pigliucci (2001) says hormones play essential role in gene-environment interaction. Then he explains how: First of all, hormones make the organism ready by genetic stimulus and they also make connection between the information of environmental receptor and genotypic specific reactions. 
 
As for understanding eukaryotic plasticity, the movement and localization of cellular components in the cell is also to be understood well (Tiedge et al 2002). According to the authors, motor proteins (myosins, dyneins, kinesins etc.) play essential role in molecular transport in the cell. Subcellular localization mechanisms of RNA in neurons are going to enlighten long-term neuronal plasticity and neurological disorders. 
 

V. Developmental and behavioral phenotypic plasticity:

 

Heterochrony is one of the mechanisms of developmental plasticity and shows variation in the timing of developmental stages (Convey and Poething 1993). According to this mechanism, the beginning of the development can be earlier or later, the development process can be slower or faster. In addition, these heterochronic events can be in combination.

 

Besides heterochrony, environmental effect-hormone interaction is crucial to understand developmental plasticity, for example temperature-dependent sex determination in reptiles (Crews et al. 1994). Instead of genetics, temperature determines the sex of the hatchling. For example, the sex of the snapping turtle is female at 23-27 0C and male at 29.5 0C. Another example of developmental phenotypic plasticity is the morphological difference when organisms are far away geographically (Mora and James 1995). The study on shell morphology of Strombus gigas displayed phenotypic differences between different places.

 

Filogamo et al (1997) studied brain plasticity. While embryonic central nervous system is developing, multi-potent cells changes to mature neurons under environmental situations. This is known as neuronal plasticity affected by neurotropic and neurotoxic factors. With aging, differentiation capacity decreases.

 

Physiological adaptation is the term that is not plasticity although developmental phenotypic plasticity can be adaptive and the best example is Daphnia (Woltereck 1909). In the presence of predator, Daphnia changes its phenotype. While physiological adaptation happens in short time, morphological plasticity needs more time. Yet, all of them change organism depending on environment. For example heat shock response is plasticity, but growth rate change in response to temperature differences is physiological response.

 

Behavior and plasticity are also two distinct terms but some behaviors, such as learning, can be more plastic than the others. Cavalli-Sforza made the first connection between behavior and plasticity (1974) and suggested to think it as similar to physiological plasticity, such as mammals change red cell quantity depending on the present oxygen and plants change photosynthesis rate depending on light. Behavioral plasticity is typical to animals. Song learning behavior is a classical example for behavioral plasticity. Ciceran et al. (1994) showed that with higher temperature while the pulse rate of Gryllus pennsylvanicus increases, on the other hand interchirp interval and chirp duration decreases. 

 

VI. Ecological significance of phenotypic plasticity: 

 
There are three types of ecological explanations for plasticity (Grime 1986): Plants can show competitive, stress tolerant or ruderal functions. Competitive function implies plants' directing their growth to nutritionally sufficient places. Stress-tolerance helps plants to survive temporarily under extreme conditions, whereas ruderal function helps plants to reproduce before stress conditions. 
 
Plasticity can be adaptive to ecology, and Ranuncula flammula is a good example for adaptive plasticity. It produces different types of leaves under and above the water (Cook and Johnson 1968). Lortie and Lonnie (1996) explained size and fecundity with adaptive plasticity. They said that evolution in a heterogeneous environment could lead a specialized or generalized adaptation. Specialized hypothesis is a null hypothesis in adaptive plasticity. Here, higher plasticity doesn't show greater adaptation but specialization. In another size-fecundity study, Clauss (1994) conducted an experiment with Arabidopsis to investigate the relationship between plant size (above ground vegetative mass excluding seeds) and fecundity (number of seeds). They found that fecundity and plant size is proportional and this relationship shows plasticity. The existence of minimum size for reproduction also indicates phenotypic plasticity. As a conclusion, the same sizes of plants in the same genotype in different environments don't show the same fecundity. They used this data to explain fitness estimates and to compare life histories of plants. 
 
Bradshaw-Sultan effect explains the stability of one trait depending on the plasticity of another developmentally related trait. Sultan (Sultan 1995) investigated three Polygonum persicaria traits under low and high light treatment and she explained the fitness of seedling biomass with the plastic change of pericarp biomass under low light. The plant keeps the stability of seedling by reducing the mass of pericarp under low light. 
 
Plasticity for plants is more important than animals since they are less mobile and helps them to modify their environment to select the most appropriate habitat (Donohue 2003). One of the example studies on plants belongs to Pigliucci (2002). He studied phenotypic plasticity in Arabidopsis. He tried to understand the ecological and environmental plasticity by studying wind effect to produce bushy phenotype in Arabidopsis. With touch response, plants are more resistant to other stresses such as herbivores. He looked at the variation between population and the plant's response to wind and predictability.
 
VII. Evolution of phenotypic plasticity:
 
Environmental heterogeneity is important for evolution of phenotypic plasticity. According to Via (1993) natural selection in heterogeneous environment causes adaptive phenotypic plasticity. How adaptive phenotypic plasticity was evolved, and how it can be measured are not clear. Environmental variation affects different phenotypic plasticity for closely related species. She argues the idea that plasticity is an independent character and says that phenotypic plasticity is not a target. Schlichting and Pigliucci (1993) argued Via's standpoint about evolution of and selection for plasticity and statistical versus genetic models.
 
Agrawal (2001) suggests that antagonistically or mutualistically, species adjust themselves to each other when they interact. This promotes evolution. Phenotypic plasticity determines the food chain, affects ecological success and evolutionary divergence, if the cost of plasticity reduces. The evolution of plasticity for some traits is not clear. 
 
Brakefield studied the variation of wing pattern as the evolution of development of plastic color patterns in response to seasonal change (Brakefield 1999). To response central focus, butterfly wings show concentric eyespot patterns. Color patterns on butterfly wings are used for species recognition, mate choice, camouflage, warning signaling, and against predator attacks.
 
The classical study on the evolutionary significance of phenotypic plasticity in plants belongs to Bradshaw (1965). He documented the examples of phenotypic plasticity in plants. For example, he mentions morphological differences between aerial and aquatic leaves. Phenotypic plasticity is specific for each character under the control of environmental effects. He suggests that specific plasticity genes control these characters. 
 
Gage (2003) investigated the evolution of human phenotypic plasticity. They studied two models. First, cost of reproduction and total nutrient flow is constantly proportional. Second, the cost of reproduction is constant for each birth. They found negative slope between age and nutritional stage.
 
To answer the question that if short term environmental change causes evolution of plasticity Leroi et al (1994) made an experiment. They used six lines of E.coli for 2,000 generations. They treated the bacteria at 32 0C and 42 0C alternatively. Then, they made the temperature change more rapidly. The new lines are better competitive to their ancestors. They concluded that these new bacteria obtained this new character by evolution. 
 
VIII. Costs and limits of phenotypic plasticity:
 
According to Newman (1992), there are limitations for plasticity: First of all, the organism might not have efficient sensory capabilities to respond the environmental change. Moreover, the organism might not be able to use its capabilities to respond the environment on time. Furthermore, due to the cost of plasticity in trait X, its contribution to trait Y decreases. Finally, reduced heritability of plasticity can cause less genetic variation. 
 
DeWitt et al. (1998) present the costs of plasticity as maintenance, production, information acquisition, developmental instability, and deleterious genetic effects. On the other hand, the study by Rick (2002) shows fitness benefits of plasticity for the first time. 
The author says that there is not much evidence that phenotypic plasticity decreases the growth. He found that plasticity affected growth positively, negatively, or showed no effect by using MANOVA test.   
 
Similarly, Chasan (1998) showed that some phenotypic plasticity types do not improve the function, but some increase the fitness. She showed that if the ratio of red is reduces at high density, Impatiens capensis plants produce long stems and if the ratio is increased by filtration, the plant produces short stems. 
 
IX. Conclusion: 
 
Although there are debates on plasticity genes, the costs of plasticity and it is difficult to study plasticity, this subject is one of the great areas to study interdisciplinary to know more about gene-environment interaction leading evolution. 
 
Beyond all of the literature, the importance of this topic is to know that it is directly proportional how much we know about life and how much we live peacefully by appreciating all of the perfect mechanisms in living organisms. One of the wonderful mechanisms in front of us waiting to enlighten our minds and hearts is plasticity. It is right there showing the beauty of variation and the meaning of trying to survive. 
 
REFERENCES

 

Agrawal, A.A. (2001) Phenotypic plasticity in the interactions and evolution of species. Science. 294(5541): 321-327.
 
Agrawal, A.A., Laforsch, C., and Tollrian, R. (1999) Transgenerational induction of defences in animals and plants. Nature 401: 60-62.
 
Bradshaw, A. D. (1965) Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115-155.

 

Brakefield, P.M. and French, V. (1999) Butterfly wings: The evolution of development of color patterns. Bioessays. 21(5): 391-402.
 
Cavalli-Sforza, L. L. (1974) The role of plasticity in biological and cultural evolution. Annals of the New York Academy of Sciences 231: 43-59.
 
Chasan, R. (1998) Plasticity lets plants soak up the sun. Bioscience 48(1): 10-12.
 
Ciceran, M., Murray, A.-M., and Rowell, G. (1994) Natural variation in the temporal patterning of calling song structure in the field cricket Gryllus pennsylvanicus: effects of temperature, age, mass, time of day, and nearest neighbor. Canadian Journal of Zoology 72:38-42.
 
Conway, L. J., and Poethig, R. S. (1993) Heterochrony in plant development. Developmental Biology 4: 65-72.
 
Cook, S. A., and Johnson, M. P. (1968) Adaptation to heterogeneous environments. I. Variation in heterophylly in Ranunculus flammula  L. Evolution 22: 496-516.
 
Crews, D. (1996) Temperature dependent sex determination: the interplay of     
steroid hormones and temperature. Zoological Science 13: 1-13.
 
Dewitt, T.J., Sih, A., and Wilson, D.S. (1998) Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77-81.
 
Donohue, K. (2003) Setting the stage: Phenotypic plasticity as habitat selection.  Int. J. Plant Sci. 164 (3): S80-94. 
 

Filogamo, G., Vernadakis, A., Gremo, F., Privat, A.M., and Timiras, P.S. (1997)

Brain Plasticity. Plenum Press, New York. 19-33.

 

Gage, T. (2003) The evolution of human phenotypic plasticity: Age and   nutritional status of maturity. Human Biology 75 (4): 521-538.
 
Grime, J. P., Crick J. C., and Rincon, J. E. (1986) Ecological significance of plasticity. Society for Experimental Biology, Great Britain.

 

Johannsen, W. (1911) The genotype conception of heredity. American Naturalist 45: 129-159.
 
Jong, de G. (1995) Phenotypic plasticity as a product of selection in a variable environment. American Naturalist 145(4): 493-513.
 
Leroi, A. M., Lenski, R.E., and Bennett, A. F. (1994) Evolutionary adaptation to temperature. III. Adaptation of E. coli to a temporarily varying environment. Evolution 48: 1222-1229.
 
Lewontin, R. C. (1974) The analysis of variance and the analysis of causes. American Journal of Human Genetics 26: 400-411.
 
Martin-Mora, E., and James, F.C. (1995) Developmental plasticity in the shell of the queen conch Strombus gigas. Ecology 76: 981-994.
 
Mitchell, R.S. (1976) Submergence experiments on nine species of semi-aquatic Polygonum. American Journal of Botany 63: 1158-1165.
 
Newman, R. A. (1992) Adaptive plasticity in amphibian metamorphosis. BioScience 42: 671-678.
 
Pigliucci, M. (1996a) How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends in Ecology and Evolution 11: 168-173.
 

Pigliucci, M. (2001) Phenotypic plasticity-Beyond nature and nurture. The John Hopkins University Press, London.

 

Pigliucci, M. (2002) Touchy and bushy: Phenotypic plasticity and integration in response to wind stimulation in Arabidopsis thaliana. Int. J. Plant Sci. 163(3):408-418.
 
Rick, R.A. (2002). Costs of phenotypic plasticity. American Naturalist. 159(3): 272-283.
 
Scheiner, S. M. and Lyman, R. F. (1991) The genetics of phenotypic plasticity. II. Response to selection. Journal of Evolutionary Biology 4: 23-50.

 

Scheiner, S. M. (1993a) Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35-68.

 

Schlichting, C.D. and Pigliucci, M. (1993) Control of phenotypic plasticity via    regulatory means. American Naturalist 142(2): 366-371. 
 
Schmalhausen, I. I. (1949) Factors of evolution: The theory of stabilizing selection. Chicago: University of Chicago Press. 
 
Sultan, S.E. (1995) Phenotypic plasticity and plant adaptation. Acta Botanica Neederlandica 44: 363-383.
 
Tiedge, H., Bloom, F.E., and Richter, D. (2002) Colloquium on molecular kinesis in cellular function and plasticity. National Academy of Sciences, USA. 6997-6998.    
 
Via, S., and Lande, R. (1985) Genotype-environment interaction and evolution of phenotypic plasticity. Evolution 39: 505-522.
 
Via, S. (1993) Adaptive phenotypic plasticity: Target or by-product of selection in a variable environment? American Naturalist 142 (2): 352-366.
 
Wu, S.-H., Wang, C., Chen, J., and Lin, B.-L. (1994) Isolation of a cDNA encoding a 70 kDa heat-shock cognate protein expressed in vegetative tissues of Arabidopsis thaliana. Plant Molecular Biology 25: 577-583.