1 Lecture 16: Phenotypic Plasticity 2 How do organisms respond to environmental change? At the individual level: Behavior Physiology Plasticity At the population level: Behavior Performance Physiology, Biochem, Morphol Plasticity 3 All of these involve complex traits Complex traits are: Common at relatively high levels of biological organization Comprised of many subordinate traits Capable of exhibiting emergent properties Often modular Affected by many genes and environmental factorsregarding human diseases and disorders 4 Emergent Properties 1noun any unique property that "emerges" when component objects are joined together in constraining relations to "construct" a higher-level aggregate object, a novel property that unpredictably comes from a combination of two simpler constituents Examples The familiar taste of salt is an emergent property with respect to the sodium and chlorine of which it is composed. 5organization-468 When units of biological material are put together, the properties of the new material are not always additive, or equal to the sum of the properties of the components. Instead, at each level, new properties and rules emerge that cannot be predicted by observations and full knowledge of the lower levels. Such properties are called emergent properties (Novikoff, 1945). Life itself is an example of an emergent property. Emergent Properties 2 6 Modularity "Although their meaning varies, modules generally are components, parts, or subsystems of a larger system that contain some or all of the following features: (i) identifiable interfaces (usually involving protocols) to other modules, (ii) can be modified and evolved somewhat independently, (iii) facilitate simplified or abstract modeling, (iv) maintain some identity when isolated or rearranged, yet (v) derive additional identity from the rest of the system." Csete, M. E., and J. C. Doyle Reverse engineering of biological complexity. Science 295: Page 1665. 7 Classic complex traits: 8 DNA Proteins, etc. Organelles Cells Tissues Organs Organ Systems Organismal Per formance Behavior The ultimate complex trait: 9 DNA Proteins, etc. Organelles Cells Tissues Organs Organ Systems Organismal Per formance Behavior Selection acts hierarchically: In animals, selection generally acts more directly on behavior than on the subordinate traits that determine performance abilities Fig. 1 in Garland, T., Jr., and S. A. Kelly Phenotypic plasticity and experimental evolution. Journal of Experimental Biology 209: 10 DNA Proteins, etc. Organelles Cells Tissues Organs Organ Systems Organismal Per formance Behavior At any level of organization... Phenotypes may be affected by environmental factors, i.e., their expression may be "plastic" 11 Phenotypic Plasticity: The ability of an individual organism to alter its phenotype in response to changes in environmental conditions. or The modification of developmental events by the environment. or The ability of one genotype to produce more than one phenotype when exposed to different environments. 12 The ability of one genotype to produce more than one phenotype when exposed to different environments. Environment Trait Environment Trait Environment Trait No PlasticityPlasticity Highly Variable Plasticity, strong Genotype-by- Environment Interaction Each of the colored lines is a "Reaction Norm" 13 1. Something in the internal and/or external environment changes (usually) 2. Organism senses that change 3. Organism alters gene expression 4. Usually, the altered gene expression yields additional observable phenotypes Features of "Phenotypic Plasticity" Includes "acclimation" and "acclimatization" as well as learning and memory. 14 1. Something in the internal and/or external environment changes (usually) Features of "Phenotypic Plasticity" Changes in ambient temperature, humidity or oxygen concentration would constitute external environmental factors, and many organisms respond to these with phenotypic plasticity that involves multiple organ systems and multiple levels of biological organization. Mechanical overload of the heart is an example of an environmental change that occurs within an organism, and it leads mainly to organ-specific changes that necessarily involve fewer levels of biological organization. 15 2. Organism senses that change Features of "Phenotypic Plasticity" Some changes may occur without any formal sensing by the organism, e.g., as a result of direct (and possibly differential) effects of temperature on the rates of ongoing biochemical and physiological processes. 16 3. Organism alters gene expression Features of "Phenotypic Plasticity" Some plastic responses need not involve changes in gene expression (transcription) but instead could occur via phosphorylation of existing proteins, changes in protein levels caused by variation in protein ubiquitination, or stimulation of existing microRNAs. 17 4. Usually, the altered gene expression yields additional observable phenotypes Features of "Phenotypic Plasticity" In principle, lower-level traits might change in offsetting ways, such that a higher-level trait could show little or no apparent change. For example, it would be theoretically possible (though perhaps unlikely) for exercise training to cause an increase in maximal heart rate but a reduction in maximal stroke volume, such that maximal cardiac output was unchanged. 18 DNA Proteins, etc. Organelles Cells Tissues Organs Organ Systems Organismal Per formance Behavior Hierarchical masking effects: Compensatory plasticity at lower levels could lead to reduced plasticity at higher levels 19 Features of "Phenotypic Plasticity" The changes may or may not be reversible. The changes may or may not be adaptive in the sense of increasing the organism's reproductive success (Darwinian fitness). The idea that environmentally induced modifications are adaptive in the sense that they improve organismal function and/or enhance Darwinian fitness has been termed the "beneficial acclimation hypothesis." In general, non-adaptive plasticity might be expected to occur any time that an organism is exposed to environmental conditions with which it is "unfamiliar" in terms of its evolutionary history. Humans taken to high altitude? Any wild animal brought into captivity? 20 Features of "Phenotypic Plasticity" In some cases, behavioral plasticity (compensation) can shield lower-level traits from selection. For example, gravid lizards or snakes may become more wary. Bauwens, D., and C. Thoen Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipera. J. Anim. Ecol. 50: Brodie, E. D., III Behavioral modification as a means of reducing the cost of reproduction. Am. Nat. 134: At the population level, phenotypic plasticity in behavior and other traits can facilitate invasions of new habitats. e.g., "willingness" to eat new foods or nest in unusual spots 21 Classic Cases of Phenotypic Plasticity Two genetically identical water fleas, Daphnia lumholtzi. The helmet and extended tail spine of the individual on the left were induced as a result of chemical cues from a predaceous fish and serve as protection. This figure is recreated from Agrawal, A Phenotypic plasticity in the interactions and evolution of species. Science 294: , Figure 1. Shown in Kelly et al. (2012) 22 Classic Cases of Phenotypic Plasticity Poorly fed and well-fed sibling echinopluteus larvae of the sea urchin Lytechinus variegatus on day 4 of development. Note greater investment in ciliated band and internal skeleton under low food conditions. Photo by J. S. McAlister. No Predator Predator 23 Classic Cases of Phenotypic Plasticity Price, T. D Phenotypic plasticity, sexual selection and the evolution of colour patterns. J. Exp. Biology 209: Carotenoid coloration is phenotypically plastic, and diets lacking carotenoids result in very little color in normally pigmented species, such as the house finch (Carpodacus mexicanus). Population differences in [carotenoid] have been related to the presence of specific food plants. 24 Taylor, C. R., and E. R. Weibel Design of the mammalian respiratory system. I. Problem and strategy. Respiration Physiology 44:1-10. Passage from page 3: We will discuss symmorphosis in a later lecture. 25 Many such examples do seem to be adaptive, i.e., to confer higher Darwinian fitness (or at least they increase organismal performance at some task), so we can proceed to ask... 26 To be or not to be: when should plasticity evolve? 27 When should plasticity evolve? Intuitively: Not in a constant environment. Not if variation in environmental factors is entirely unpredictable. In those cases, the optimum genotype is likely to be one that results in a single phenotype that confers high Darwinian fitness with respect to the long-term average environmental conditions. 28 Formal Theoretical Models: "As a null model I assume that plasticity is not costly.... costs would usually enter as constant factors that do not alter the optimal values of mode and breadth." Gabriel, W How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18: 29 Gabriel, W How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18: "Phenotypic plasticity... can be an adaptive strategy to cope with variable environments... and is a common phenomenon for many traits in almost all organisms." "Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays." Implicitly, he seems to define "stress" as anything that threatens homeostasis, survival or other components of Darwinian fitness. 30 "Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non- induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions." Gabriel, W How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18: 31 Gabriel's (2005) Conclusions: "reversible phenotypic plasticity would be expected for all organisms [if ]: they are exposed to stress periods that last shorter than life span; stress appears in the long run with some regularity so that natural selection can shape... plastic traits. Are these predictions supported?... given the predicted huge fitness advantages, the cost of plasticity would have to be unexpectedly high... to counteract selection for reversible... plasticity." 32 Ways to study evolution: Compare extant species (or populations) to infer what has happened in the past... 33 Environmental Variability Plasticity Ways to study evolution: 34 Comparisons of Species: Valladares, F., S. J. Wright, E. Lasso, K. Kitajima, and R. W. Pearcy Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81: Mean Plasticity Understory Gap More Variable Less Variable 35 Comparisons of Species: Valladares, F., S. J. Wright, E. Lasso, K. Kitajima, and R. W. Pearcy Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81: Mean Plasticity Understory Gap More plastic for gas exchange traits than for structural traits 36 Comparisons of Species: Some generalities: Plant morphology is more plastic than animal morphology. In animals, behavior is very plastic. In vertebrates, skeletal muscle is more plastic than the lung. Skeletal muscle is more plastic in mammals than in lizards. Snake guts are very plastic. Carp are very plastic. 37 Comparisons of Species: Fig. 1. Small intestinal wet mass, intestinal nutrient uptake rates, and intestinal nutrient uptake capacity of fasted snakes presented as a percentage of those variables measured from digesting individuals of four species of infrequently-feeding snakes (A) and of four species of frequently-feeding snakes (B). For nutrient uptake rates and uptake capacities, bars represent the average fasted percentages (+ SE) for the uptake of L- leucine, L-proline, and D-glucose. Note that with fasting infrequently-feeding snakes reduce intestinal mass, nutrient uptake rates, and therefore uptake capacity by much greater magnitudes than frequently-feeding species. Source of data is Secor and Diamond (2000). From Secor (2005) Integr. Comp. Biol. 45: 38 Comparisons of Species: Fig. 3. Phylogenetic assessment of the postprandial increase in intestinal nutrient uptake capacity for 24 families and 4 subfamilies of amphibians and reptiles. Bar lengths represent the mean factorial increase for the uptake capacity of L- leucine, L-proline, and D-glucose. For families represented by multiple species (see Table 1), bar length and error bars signify mean and 1 SE of averaged factorial increase in uptake capacities among those species. From Secor (2005) Integr. Comp. Biol. 45: 39 Generation Body Mass (g) 30 grams 67 grams The longest- running ver tebrate ar tificial selection experiment: Male mice at 42 days of age 100 gens. Bunger, L., A. Laidlaw, G. Bulfield, E. J. Eisen, J. F. Medrano, G. E. Bradford, F. Pirchner, U. Renne, W. Schlote, and W. G. Hill Inbred lines of mice derived from long-term growth selected lines: unique resources for mapping growth genes. Mammalian Genome 12: Another way to study evolution: Impose selection in an experimental population and observe evolution in real time... 40 Example: Selection on Plasticity Scheiner, S. M., and R. F. Lyman The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4: Difference in thorax size of Drosophila melanogaster at 19 & 25 o C "We used a family selection scheme to select on the trait of phenotypic plasticity of thorax size in response to temperature. That is, the phenotype of a group of full-sibs as expressed in two environments was the selected trait. We realize that this form of selection will not be the usual form of selection in nature. However, the purpose of this experiment was to explore aspects of the genetic basis of the trait rather than to mimic natural selection." 41 Example: Selection on Plasticity Scheiner, S. M., and R. F. Lyman The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4: Difference in thorax size of Drosophila melanogaster at 19 & 25 o C 42 Example: Selection on Plasticity Scheiner, S. M., and R. F. Lyman The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4: Difference in thorax size of Drosophila melanogaster at 19 & 25 o C "We have demonstrated that phenotypic plasticity is a trait that can respond to selection. This response is partially independent of change in the mean of that trait; selection on plasticity of thorax size did not result in a change in mean thorax size but selection on mean thorax size did change plasticity. The complex pattern of direct and correlated responses to selection show that the phenotypic plasticity of a trait can be considered a character upon which evolution can act but in ways which will interact with selection on the mean of the trait." 43 Scheiner, S. M., and R. F. Lyman The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4:23-50. 44 Plasticity may also evolve even when it is not an intentional target of selection. Any time the selective event is more than instantaneous, plasticity may evolve. For example, many selection experiments with Drosophila involve desiccation, temperature or starvation "stress" that lasts for hours or days. Survivors may be those that were innately more tolerant at the start of the stress and/or that rapidly increased their tolerance. 45 Example: Selection Not on Plasticity Harshman, L. G., J. A. Ottea, and B. D. Hammock Evolved environment-dependent expression of detoxication enzyme activity in Drosophila melanogaster. Evolution 45: Reared on standard medium (3 Control lines) or lemon (3 Selected lines) for 20 generations. For the Selected lines: 1. flies were placed in bottles with fresh lemon for 7-10 days; 2. 50% mortality occurred; 3. survivors were placed into a new bottle with fresh lemon and vermiculite to produce the next generation. All test flies were reared on standard medium for 1 generation. All were transferred to either lemon or fresh medium for 24 h. Epoxide hydrolases and glutathione S-tranferase assayed. 46 Example: Selection Not on Plasticity Control Selected Greater Induction Interaction P = = "Genotype-by-Environment Interaction" 47 Harshman, L. G., J. A. Ottea, and B. D. Hammock Evolved environment-dependent expression of detoxication enzyme activity in Drosophila melanogaster. Evolution 45: Example: Selection Not on Plasticity "In the present study the culturing regime used was ostensibly continuous, unless the process of lemon rotting every generation constitutes temporal variation. Normally, one would anticipate selection for change in environment-dependent enzyme expression to occur in variable environments but the results of the present study suggest it can evolve in a relatively constant regime." 48 "Self-Induced Adaptive Plasticity" Swallow, J. G., J. S. Rhodes, and T. Garland, Jr Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integrative and Comparative Biology 45: A behavior under selection causes changes in subordinate traits that in turn enhance the ability of the organism to perform the behavior. 49 "Self-Induced Adaptive Plasticity" Possible examples in nature: Animals that feed on particular foods may experience shifts in digestive enzymes that facilitate their ability to eat those foods. Birds that engage in altitudinal migration might make "trial runs" that would induce physiological changes that would improve their ability to function at high altitude. In rats, maternal behavior is hormone-dependent in first- time mothers, but is less so in experienced mothers. Similarly, male-male agonistic interactions in vertebrates may result in the winners experiencing elevated testosterone levels, which could facilitate their subsequent performance in such interactions. 50 ExtraSlidesFollow 51 This was about 20 minutes short in Add more real examples, e.g., Hicks snake guts and hearts. Human/rat training studies. For 2012, I added Dapnia picture from Kelly et al. (2012) CPHY paper and also Secor on snake guts. It was then just about right on time. However, in 2013 it was about 8 minutes too short. Includes "acclimation" and "acclimatization" as well as learning and memory. For 2014, it was 15 min short??? For 2015, need to move GLUT4 plasticity into here - Ted forgot to do this! 52 Example: Selection Not on Plasticity 53 Updates for 2007 Winter: Pigliucci, M. Phenotypic plasticity 101. FromPigliucci, M Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20: 54 Gomez-Mestre, I., and D. R. Buchholz Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proceedings of the National Academy of Sciences, USA 103: Developmental plasticity is found in most organisms, but its role in evolution remains controversial. Environmentally induced phenotypic differences may be translated into adaptive divergence among lineages experiencing different environmental conditions through genetic accommodation. To examine this evolutionary mechanism, we studied the relationship between plasticity in larval development, postmetamorphic morphology, and morphological diversity in spadefoot toads, a group of closely related species that are highly divergent in the larval period and body shape and are distributed throughout temperate areas of both the New and the Old World. Previous studies showed that accelerated metamorphosis is adaptive for desert- dwelling spadefoot toads. We show that even under common garden conditions, spadefoot toad species show divergent reaction norms for the larval period. In addition, experimentally induced changes in the larval period caused correlated morphological changes in postmetamorphic individuals such that long larval periods resulted in relatively longer hindlimbs and snouts. A comparative analysis of morphological variation across spadefoot toad species also revealed a positive correlation between the larval period and limb and snout lengths, mirroring the effects of within-species plasticity at a higher taxonomic level. Indeed, after 110 Ma of independent evolution, differences in the larval period explain 57% of the variance in relative limb length and 33% of snout length across species. Thus, morphological diversity across these species appears to have evolved as a correlated response to selection for a reduced larval period in desert-dwelling species, possibly diverging from ancestral plasticity through genetic accommodation. 55 "Self-Induced Adaptive Plasticity" Swallow, J. G., J. S. Rhodes, and T. Garland, Jr Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integrative and Comparative Biology 45: The behavior under selection causes changes in subordinate traits that in turn enhance the ability of the organism to perform the behavior. Could be a threshold effect, could be quantitative within both linetypes, or could be difference between S and C (like neurogenesis) As wheel running increases across generations, that leads to greater training effects, which in turn support the higher wheel running. 56 When should plasticity evolve? Gabriel, 2005: "Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays.... Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions." 57 58 Experimental Evolution: "By experimental evolution we mean research in which populations are studied across multiple generations under defined and reproducible conditions, whether in the laboratory or in nature." 59 Possible wheel-running trajectories: Selected Control Day S/C = 3 on days 2- 6 60 JEB Discussion Meeting - "Phenotypic Plasticity" Hans Hoppeler, Ken Lukowiak, M. Flueck, and Ewald R. Weibel Downing College, Cambridge UK September , 2005 Goal and Structure of Conference Phenotypic plasticity is a fundamental biological phenomenon common to all organisms. Phenotypic plasticity allows individuals of a species to adapt to environmental challenges and thus to improve fitness and eventually reproductive success. Over the last decade the mechanisms of phenotypic plasticity have become a very active area of (comparative) biological research. It looks like an excellent time to look at Phenotypic Plasticity in terms of its structural and physiological expression as well as the molecular mechanisms that drive it. The symposium brings together scientists of diverse orientations, from molecular biology to comparative physiology and ecology, engaged in both experimental and theoretical work. It offers a platform for the open discussion of concepts and observations on the variation in diverse biological processes associated with phenotypic plasticity. Each of the four sessions has four speakers with 25 minutes of lecture and 10 minutes discussion each. The session is concluded with a general discussion period of 20 minutes. Participation is by invitation only. 61 Phenotypic plasticity of skeletal muscle. Chair: Hoppeler Flueck M Functional, structural and molecular plasticity of mammalian skeletal muscle Johnston IA Environment and the plasticity of skeletal muscle in fish Hood DA Coordination of metabolic plasticity in skeletal muscle Anderson JE The satellite cell in skeletal muscle plasticity General Discussion Sunday 62 Phenotypic plasticity of the brain. Chair: Lukowiak Nguyen PV Comparative plasticity of brain synapses in inbred mouse strains Magistretti PJ Neuron-glia metabolic coupling and plasticity Weiss S Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin Syed NI The brain plasticity at the base of neuron silicon interface General Discussion Sunday 63 Molecular mechanisms of phenotypic plasticity. Chair: Flueck Swynghedauw B Phenotypic plasticity of adult myocardium. Molecular mechanisms Cossins AR Genomic insights into the mechanisms of environmentally-induced phenotypic plasticity Schrader J Molecular strategies compensating loss of gene function: lessons from the myoglobin knockout mice Goldring CE Plasticity in cell defence: access to and reactivity of critical protein residues and DNA response elements General Discussion Monday 64 Role of phenotypic plasticity in evolution. Chair: Garland Fordyce JA The evolutionary consequences of ecological interactions mediated through phenotypic plasticity Garland T Jr Phenotypic plasticity and experimentalevolution Pigliucci M Evolution by genetic assimilation: much ado about nothing? Price TD Phenotypic plasticity and the evolution of colour patterns General Discussion and End of Conference Tuesday 65 Crucial Point! Any particular instance of phenotypic plasticity may or may not be adaptive! However, many examples do seem to be adaptive (i.e., to confer higher Darwinian fitness), so we can proceed to ask...