Understanding Phenotypic Plasticity in Response to Environmental Change

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 factors http://complextrait.org/ regarding human diseases and disorders

4. Emergent Properties 1 http://dictionary.reference.com/browse/emergent+property noun 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.

5. Emergent Properties 2 http://www.nature.com/scitable/topicpage/biological-complexity-and-integrative-levels-of-organization-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.

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. 2002. Reverse engineering of biological complexity. Science 295:1664-1669. Page 1665.

7. Classic complex traits:

8. Behavior OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA The ultimate complex trait:

9. Behavior OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA 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. 2006. Phenotypic plasticity and experimental evolution. Journal of Experimental Biology 209:2234-2261.

10. Behavior OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA 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. Trait Trait Trait Environment Environment Environment The ability of one genotype to produce more than one phenotype when exposed to different environments. Highly Variable Plasticity, strong Genotype-by-Environment Interaction No Plasticity Plasticity Each of the colored lines is a "Reaction Norm"

13. Features of "Phenotypic Plasticity" 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 Includes "acclimation" and "acclimatization" as well as learning and memory.

14. Features of "Phenotypic Plasticity" 1. Something in the internal and/or external environment changes (usually) Changes in ambient temperature, humidity oroxygen 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. Features of "Phenotypic Plasticity" 2. Organism senses that change 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. Features of "Phenotypic Plasticity" 3. Organism alters gene expression 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. Features of "Phenotypic Plasticity" 4. Usually, the altered gene expression yields additional observable phenotypes 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. Behavior OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA 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. 1981. Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipera. J. Anim. Ecol. 50:733-743. Brodie, E. D., III. 1989. Behavioral modification as a means of reducing the cost of reproduction. Am. Nat. 134:225-238. 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. 2001. Phenotypic plasticity in the interactions and evolution of species. Science 294:321-326, Figure 1. Shown in Kelly et al. (2012)

22. No Predator Predator http://www.zoo.ufl.edu/mccoy/Quantifyingplasticity.htm 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. http://www.unc.edu/~podolsky/plasticity.htm

23. Classic Cases of Phenotypic Plasticity 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. Price, T. D. 2006. Phenotypic plasticity, sexual selection and the evolution of colour patterns. J. Exp. Biology 209:2368-2376.

24. Taylor, C. R., and E. R. Weibel. 1981. 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 shouldplasticity 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: Gabriel, W. 2005. How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18:873-883. "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."

29. Gabriel, W. 2005. How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18:873-883. "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. Gabriel, W. 2005. How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18:873-883. "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."

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. ... given the predicted huge fitness advantages,the cost of plasticity would have to be unexpectedly high ... to counteract selection for reversible ... plasticity." Are these predictions supported?

32. Ways to study evolution: Compare extant species (or populations)to infer whathas happenedin the past ...

33. Plasticity Environmental Variability Ways to study evolution:

34. Comparisons of Species: More Variable Less Variable UnderstoryGap Mean Plasticity Valladares, F., S. J. Wright, E. Lasso, K. Kitajima, and R. W. Pearcy. 2000. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925-1936.

35. Comparisons of Species: More plastic for gas exchange traits than for structural traits Understory Gap Mean Plasticity Valladares, F., S. J. Wright, E. Lasso, K. Kitajima, and R. W. Pearcy. 2000. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925-1936.

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. 45:282-294

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. 45:282-294

39. 67 grams Body Mass (g) 30 grams Generation Another way to study evolution: Impose selection in an experimental population and observe evolutionin real time ... Male miceat 42 days of age The longest- runningvertebrateartificial selection experiment: 100gens. 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. 2001. Inbred lines of mice derived from long-term growth selected lines: unique resources for mapping growth genes. Mammalian Genome 12:678-686.

40. Example: Selection on Plasticity • Scheiner, S. M., and R. F. Lyman. 1991. The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4:23-50. • Difference in thorax size of Drosophila melanogaster at 19 & 25oC • "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. 1991. The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4:23-50. Difference in thorax size of Drosophila melanogaster at 19 & 25oC

42. Example: Selection on Plasticity • Scheiner, S. M., and R. F. Lyman. 1991. The genetics of phenotypic plasticity. II. Responses to selection. J. Evol. Biol. 4:23-50. • Difference in thorax size of Drosophila melanogaster at 19 & 25oC • "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. 1991. 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. 1991. Evolved environment-dependent expression of detoxication enzyme activity in Drosophila melanogaster. Evolution 45:791-795. 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. Interaction P = 0.0068 Greater Induction Example: Selection Not on Plasticity = "Genotype-by-Environment Interaction" ControlSelected

47. Example: Selection Not on Plasticity Harshman, L. G., J. A. Ottea, and B. D. Hammock. 1991. Evolved environment-dependent expression of detoxication enzyme activity in Drosophila melanogaster. Evolution 45:791-795. "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. 2005. Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integrative and Comparative Biology 45:426-437. 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.

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