The Evolution of Plasticity & Learning

The Evolution of Plasticity & Learning E3: Lecture 17

Phenotype versus Genotype • Even before the rediscovery of Mendel’s results, August Weismann proposed the separation of germ cells and somatic cells. The former carried the hereditary material and the latter performed various body functions. • Mendel’s famous experiments with peas suggested the existence of discrete particles of inheritance (this was the best way to explain the reemergence of a phenotype in the F2 generation not found in the F1 generation). • Not long after the rediscovery of Mendel’s work, Wilhem Johannsen introduced the terms “genotype” and “phenotype” to refer to the composition of the hereditary particles and the physical appearance of the organism (in which environmental influences played a role). August Weismann   P F1 yy Yy Yy YY Gregor Mendel YY F2 Yy yy F1 Yy 100% 25% 75% Wilhem Johannsen

Nature versus Nurture • In 1581, educator Richard Mulcaster wrote about “abilities …what were in children, by nature emplanted, for nurture to enlarge.” • The roles of genotype versus environment in producing phenotype echoes a long-standing debate over the importance of “nature” versus “nurture” • Certain phenotypic traits (e.g., eye color) seem fairly insensitive to environmental differences but fairly sensitive to genetic differences (nature over nurture). • Other phenotypic traits (e.g., spoken language) seem fairly insensitive to genetic differences, but fairly sensitive to environmental differences (nurture over nature). • Of course, any phenotypic trait is influenced by both genetic and environmental factors, but… • Why might certain traits show more flexibility with differences in one factor over the other? • Is there a general framework in which we can dissect the influence of various factors?

The Evolution of Plasticity & Learning • Lecture Outline • Introduction to phenotypic plasticity • Experimental investigation of plasticity • Learning as a form of plasticity • Experimental evolution on learning • Summary

Genotype Does Not Completely Determine Phenotype • Organisms do not develop in a vacuum; their environment can be critical to their development. Thus, the same genotype can look different in different developmental environments. • Examples of sensitivity to the environment: • The butterfly Bicyclus anynana has both a dry-season morph (dull brown without dramatic eye-spots) and a wet-season morph (with a set of eye-spots and bands). • The annual plant Impatiens capensis will exhibit elongated stems under low red:far-red (R:FR) light ratios relative to high R:FR growth conditions. • The barnacle Chthamalus anisopoma curves its shell when a gastropod predator is present during its development wet season dry season low R:FR ratio high R:FR predator no predator

A Cooked-Up Analogy • Consider again our butterfly that exhibits polyphenism (multiple morphs). • In this case, the heriditary material (e.g., genes) does not completely specify the wing pattern; rather environmental influences (e.g., temperature) are crucial. • As an analogy, consider the way a cake looks and tastes. • A recipe alone does not bake the cake; moreover, different cakes can be made using the same recipe if the “environment” changes (e.g., cook, oven, ingredients, etc.) inherited material environment recipe cake’s “environment”

Phenotypic Plasticity • When a given genotype produces different phenotypes under different environmental circumstances, the genotype is termed plastic • This is represented by the genotype’s norm of reaction, a function that relates the developmental environment to the phenotype produced. • A flat norm of reaction represents a relatively non-plastic genotype; whereas a steep norm of reaction represents a genotype that is phenotypically sensitive to the environment. • For instance, the size of barking tree frogs at metamorphosis declines with temperature, whereas the squirrel tree frog seems less plastic. genotype A genotype B phenotype genotype C environment Hyla gratiosa size at metamorphosis Hyla squirella temperature

Nature versus Nurture: Revisited • If different genotypes give different (environment-independent) phenotypes (e.g. a series of flat displaced norms of reaction), this corresponds to a situtation in which “nature” is given causal power. • If different genotypes give the same (environment-dependent) phenotypes (e.g., a series of non-flat completely overlapping norms of reaction), this corresponds to a situation in which “nurture” is given causal power. • There are two important things to note: • The situations in which either of these situations strictly apply are few and far between. • All statements of nature (e.g., genetic, innate, inherited, inborn, etc.) and nurture (e.g., environmental, learned, experiential, etc.) are relative to the set of genotypes, environments and phenotypes measured. genotype A genotype B phenotype genotype C environment genotype A genotype B phenotype genotype C environment

Why Be Plastic? Dry morph→Camoflauge in dry litter during inactive season Wet morph→Eyespots “deflect” predators during active season wet season dry season brightness of eye spots temperature Brakefield & French 1999 Tall plant→Advantageous to elongate when shaded out by neighbors Short plant→Advantageous to avoid elongation when light is abundant low R:FR ratio high R:FR plant height Dudley & Schmidt 1996 R:FR ratio Unbent morph→More fecund without predators present Bent morph→Physically deters predation by gastropods predator no predator shell curvature predator density Lively 1986

Plasticity Need Not be Adaptive Very dull eye spots (on a very dull butterfly) • Phenotypic plasticity may not be adaptive. • Consider our butterfly again • The brightness of the eye spots also changes at 100C, but it would be hard to call this adaptive… brightness of eye spots 18C 24C 100C temperature Take 5 minutes to talk to your neighbor about the following: Assume you have found plasticity in a species you are studying in response to some environmental cue. How might you experimentally demonstrate that the plasticity is adaptive? shady sunny dry wet no predator predator

Addressing the Adaptive Value of Plasticity • For plasticity to be valuable, the following should apply: • The environment should be heterogeneous • There should be no single phenotype that is optimal in all environments (i.e., what works in one environment does not work in another). • The environmental cue for development should be a reasonable predictor of later fitness of the phenotype. • One experimental approach to addressing the adaptive value of plasticity involves the separation of the developmental environment from the selective environment. plant height R:FR ratio developmental environment selective environment high density low density

Plasticity Experiment ambient light filtered light Susan Dudley Johanna Schmitt • Dudley & Schmitt (1996) tested whether elongation in Impatiens capensis is adaptive. • By filtering light, they grew plants under two different developmental environments: Elongation (low R:FR) and Suppression (high R:FR). • By transplanting plants from different cue environments to both low and high density selective environments, the fitness of different phenotypes could be gauged. developmental environment Suppression treatment Elongation treatment selective environment Low density treatment High density treatment

Demonstration of Adaptive Plasticity • The authors measured the total number of reproductive structures (flowers, fruits, and pedicels) produced by each plant in the selective environments. • They found that elongated plants had higher fitness at high density; whereas suppressed plants had higher fitness at low density. • These findings are consistent with an adaptive form of plasticity: Elongation is valuable in high density (in order to gather light), but detrimental when sufficient light is available. Elongated -High Suppressed -High Elongated -Low Suppressed -Low

Adaptive Shade Avoidance • For plasticity to be valuable, the following should apply: • The environment should be heterogeneous These annual plants live in both woodland and open habitats where light levels vary. • There should be no single phenotype that is optimal in all environments (i.e., what works in one environment does not work in another). Dudley & Schmitt experimentally demonstrated that each environment has a different optimal phenotype. • The environmental cue for development should be a reasonable predictor of later fitness of the phenotype. Low R:FR ratios are found in dense patches of competitors (where elongation is likely to pay off). High R:FR ratios are found in open patches (where suppression pays off). plant height R:FR ratio

Types of Plasticity • Phenotypic plasticity can be adaptive (e.g., shade avoidance) or non-adaptive (e.g., cooked butterflies) • Phenotypic plasticity can also be either reversible or irreversible. • Reversible plasticity occurs when different phenotypes are continually expressed throughout the lifetime (e.g., lac operon) • Irreversible plasticity occurs when phenotypes become fixed after a critical window (e.g., wing pattern) • One type of very special reversible plasticity is neuronal-based learning. adaptive plasticity non-adaptive plasticity brightness of eye spots plant height R:FR ratio 24C 100C temperature reversible plasticity irreversible plasticity brightness of eye spots lac expression t=1 t=1 glucose lactose 18C 24C temperature brightness of eye spots lac expression t=10 t=10 glucose lactose 18C 24C temperature

Learning: Building Your Reaction Norm • Learning can be a tremendously effective way to approach a changing or novel world. • Consider the case of Betty the crow: • This crow learned to fashion a hook into a wire in order to grasp a handle of a bucket of food. • What Betty and other animals are able to do is build a reaction norm through experience: • Stimuli are the “environment” • Behavior is the “phenotype” • This is a case of reversible plasticity (e.g., different stimuli are continually able to elicit different responses), but also this is a case where the very nature of the plasticity can change over time. 3 2 1

The Crow’s Urban Nutcracker

Why Learn? • As with the early argument about plasticity, learning should be adaptive when: • The environment changes over time • There is no single behavior that is optimal in all environments (i.e., what works for one stimulus at a given time does not necessarily work for another stimulus). • A given behavioral response to a given stimulus is reasonably reliable over time. • The rate of change in the environment (i.e. stimuli) is important to the value of learning: • If the environment changes too slowly, then innate behaviors may be favored • If the environment changes too quickly, then what is learned today has no use tomorrow. • Environmental change needs to be “just right”–models have shown that low rates of change within generations and high rates of change between generations are ideal. t=1 t=24 Goldilocks Principle

Learning Experiment Trial 1 Gen i Trial 1 Gen i+1 Tadeusz Kawecki Frederic Mery Q Q • Mery & Kawecki (2002) explored real-time evolution of learning in D. melanogaster. • Within each generation in their treatment, they paired one of two fruit flavors with an aversive chemical cue (quinine) during a “learning trial” • They removed the cue during subsequent “selection trials,” picking eggs from the flavor not previously associated with quininefor the next generation. • Quinine-paired flavors alternated between generations; whereas control populations lacked quinone. Trial 2 Gen i Trial 2 Gen i+1 Trial 3 Gen i Trial 3 Gen i+1

Measuring Learning: Conditioning Response • The authors split the lines into three treatments to test for conditioning effects: • Quinine paired with pineapple in first trial • Quinine paired with orange in first trial • No quinine in first trial (used to measure “preference”) • Number of eggs on each agar flavor (without quinine) from the third trial were scored. • They also did this with two new flavors (tomato and apple), using the same design. Trial 1 Trial 1 Trial 1 Trial 1 Q Q Q Trial 3 Trial 3 Trial 3 Trial 3

Measuring Learning: Rate • The authors split the experimental and control lines into groups exposed to a quinine-paired flavor for variable amounts of time: • Number of eggs on each agar flavor (without quinine) from a choice Trial were scored. Q Q Q Q Q Q

Measuring Learning: Memory • The authors split the experimental and control lines into groups exposed to a quinine-paired flavor for a set amount of time and then variably delayed the time until the choice. • Number of eggs on each agar flavor (without quinine) were scored. 1 hr Q Q Q 2 hrs Q Q Q 3 hrs Q Q Q

The Evolution of Learning • The experimental flies showed preferential egg laying in the medium not paired with quinine. • Response to conditioning: Experimental flies showed strong increases in oviposition on the flavor not originally paired with quinine (whereas the control and stock flies did not); this result held for novel flavors too. • Rate of learning: Experimental flies showed a stronger aversion away from the previously quinine-paired flavor with shorter forced exposure to it. • Decay of conditioned response: The decay of conditioning was faster in the control flies than in the experimental flies. Q- Q- Q- Q- Q- Q-

Adaptive Learning • Learning should be adaptive when: • The environment changes over time The flavor paired with quinine was alternating in the experiment. • There is no single behavior that is optimal in all environments Flies in the experimental treatment could not always simply avoid a single flavor. • A given behavioral response to a given stimulus is reasonably reliable over time. Avoiding the flavor that was paired with quinine gave a reliable prediction of fitness (as eggs were selected from the alternative flavor). • Mery & Kawecki found that under their experimental treatment (relative to their control), flies evolved a faster rate of learning, a longer memory and a pronounced conditioned response in avoiding a flavor paired with an aversive cue. Take 5 minutes to talk to your neighbor about the following: What might be potential costs to learning? How might you experimentally test for these costs? Could you use Mery & Kawecki’s system to do this?

Summary • Organismal development is generally influenced by environmental inputs– such sensitivity is termed phenotypic plasticity and is represented graphically by the norm of reaction (a genotype-specific graph giving phenotype as a function of environment). • Plasticity can be irreversible or reversible (this depends on whether continual changes in environmental exposure produce changes in phenotype). Morphological development in animals is often irreversible, whereas physiological reactions are often reversible. • Neuronal-based learning is a special type of reversible plasticity. • Whether plasticity and learning is adaptive depends on a number of factors: the costs of plasticity, heterogeneity in the environment, reliability in cues, and phenotypic trade-offs. • Experimentalists have shown shade avoidance plasticity to be adaptive in annual plants and learning to evolve de novo in fruit flies.

The Evolution of Plasticity & Learning