Environmental variation favors the evolution of variable phenotypes

As we saw at the beginning of this chapter, survival and growth of treefrog tadpoles depend on the environmental conditions that they experience and on how they alter their phenotype in response. As we have noted in earlier chapters, all phenotypes are the product of genes interacting with environments. As a result, environmentally induced traits have a genetic basis, but reflect the ability of the environment to turn certain genes on or off, which causes different phenotypes to develop. The environments that induce these changes may change so rapidly that they occur within a generation or they may be somewhat slower and vary across generations. The experience of the tree frog is a good example; predators and competitors can differ substantially from pond to pond in a particular year, from year to year in a particular pond, and even from week to week during the time it takes for a generation of tadpoles to metamorphose and leave the pond as frogs. In this section we will examine how producing different phenotypes can be an effective strategy in changing environments. We will also examine the importance of reliable environmental cues, the speed at which different traits can change, and whether environmentally induced phenotypes can be reversed.

Phenotypic Tradeoffs

In Chapter 2 we saw that rainbow trout that express cold-water isozymes in their tissues perform well in cold water and poorly in warm water. In contrast, fish expressing warm-water isozymes perform well in warm water and poorly in cold water (Figure 2.20). Throughout the natural world we see that a phenotype that is well-suited to one environment may be poorly suited to other environments.

Figure 4.4 illustrates phenotypic fitness in relation to environment. In Figure 4.4a, an individual possessing phenotype X is well suited to environment X and therefore experiences high fitness. In environment Y, however, the phenotype is no longer well suited to the environment and it therefore experiences reduced fitness. In contrast, an individual that possesses phenotype Y is well suited to environment Y and experiences high fitness in environment Y. However, it is poorly suited to environment X, so it experiences reduced fitness in environment X. When a given phenotype experiences higher fitness in one environment whereas other phenotypes experience higher fitness in other environments, we say that there is a phenotypic trade-off, meaning that neither phenotype does well in both environments.

Figure 4.4 Environments, phenotypes, and fitness. Different environments cause phenotypes to experience different amounts of fitness. (a) Phenotypic plasticity evolves because a phenotype has high fitness in one environment and low fitness in another environment. (b) Given this trade-off, nonplastic genotypes have high fitness in one environment but low fitness in other environments. In contrast, a plastic genotype can have high fitness in both environments. (c) If we consider the average fitness across both environments, we see that the plastic genotype experiences higher average fitness than either of the two nonplastic genotypes.

But what if an individual could produce a range of phenotypes and each phenotype could perform well in a specific environment? Individuals with mutations that allow them to produce unique phenotypes suited to different environments would experience high fitness in both environments and therefore be favored by natural selection. The ability of a single genotype to produce multiple phenotypes is called phenotypic plasticity. Phenotypic plasticity is a widespread phenomenon in nature; nearly every organism—bacteria, protists, plants, fungi, and animals—possesses phenotypically plastic traits. Different traits can change at different rates and these environmentally induced traits can be either reversible or irreversible. By changing its traits, an individual often maintains a high level of performance when the environment changes. This means that phenotypically plastic traits often are a mechanism of achieving homeostasis, a concept we discussed in Chapter 3.

Figure 4.4b shows the advantage of being phenotypically plastic. In contrast to the two nonplastic genotypes, labeled as genotype X and genotype Y, the plastic genotype, labeled as genotype Z, has a relatively high fitness in both environments because it can produce a phenotype that is nearly as fit as genotype X in environment X and a phenotype that is nearly as fit as genotype Y in environment Y. If we examine the average fitness of the three different genotypes in Figure 4.4c, we see that it is higher for the plastic genotype. Whenever environmental variation coincides with phenotypic trade-offs across different environments, natural selection will favor the evolution of phenotypic plasticity.

For a long time, scientists applied the concept of phenotypic plasticity to certain types of traits, such as changes in morphology or physiology. However, scientists now recognize that many other types of traits—for example, behavior, growth, development, and reproduction—frequently represent alternative phenotypes that can change under different environmental conditions. As a result, the conceptual framework of phenotypic plasticity has expanded in recent years to consider all of these types of traits.

We can see the advantage of phenotypic plasticity in the example of the gray treefrog tadpoles discussed at the beginning of this chapter. In environments with predators, the tadpoles produce a phenotype that is well suited to escape. However, the cost of this phenotype is slower growth. In predator-free environments, the tadpoles produce a different phenotype that is well suited for faster growth. However, the cost of this phenotype is increased vulnerability to predators. With only one possible phenotype, the tadpoles would perform poorly whenever the environment changed. In contrast, a tadpole that can change its behavior and body shape performs relatively well when the environment changes.

The fitness advantage of phenotypic plasticity occurs whenever environmental variation in space or time occurs frequently. If environmental conditions frequently change, then the phenotype favored by natural selection also changes frequently and this gives the plastic genotype a higher average fitness than the nonplastic genotype. If spatial or temporal variation is not common, a single phenotype will be favored; the nonplastic genotype that has the highest fitness in the stable environment will be favored if it has a higher fitness than a plastic genotype.

Environmental Cues

For an organism to alter its phenotype in an adaptive way, it must first be able to sense its environmental conditions. For example, the gray treefrog tadpole first senses whether the pond contains predators or competitors and then alters its phenotype to improve fitness. As we will see throughout the rest of this chapter, environmental cues can take many forms, including smells, sights, sounds, and changes in abiotic conditions. Of the numerous potential cues an organism might use, the best are those that offer the most reliable information about the environment. For example, an organism that requires a reliable cue about competition for food could use the presence of a large number of conspecifics—members of its own species—that will be eating the same thing. But if ample food is available, even a large number of conspecifics would not result in competition for food and would be a poor indicator of the level of competition. A better environmental cue of competition for food might be the amount of food that an individual can acquire each day. In an environment with high competition, an individual will always experience a decline in the amount of food available per day. Therefore, the daily intake of food is a more reliable indicator of high competition than the number of conspecifics. When organisms have very reliable cues, they can more accurately produce a phenotype that is well suited to the environment.

Response Speed and Reversibility

Phenotypically plastic traits respond to changes in the environment at different rates. Some of the trait changes are irreversible. The most rapid responses are typically behavioral traits, which can be altered in seconds. For example, most prey rapidly respond to a predator’s pursuit; often it takes less than one second for the prey to flee. Physiological plasticity, which is an environmentally induced change in an individual’s physiology—sometimes referred to as acclimation—can also be relatively rapid. Consider the time it takes humans to acclimate to the low-oxygen conditions that are caused by lower air pressures at high altitudes, or the time required for human skin to tan. Both of these physiological changes can be accomplished in just a few days. In contrast to these behavioral and physiological changes, changes in morphology—including changes in body shape and the size of internal organs—and changes in life history—including time to sexual maturity and number of progeny produced—can take considerably more time, often on the scale of weeks, months, or years.

Differences in response speed have implications for the reversibility of the induced traits. Behavioral traits that are induced by a change in the environment typically can be rapidly reversed if the environment reverts to its original condition. For example, an animal can quickly and easily adjust its food intake as food conditions change over time. Induced changes in morphology and life history are more difficult to reverse. For many organisms such as plants, changes in morphology are difficult or impossible to undo. For example, plants commonly respond to low light conditions by growing taller in an attempt to rise above neighboring plants that are casting shade. If the environment suddenly becomes sunny, a plant cannot make itself shorter. Even less reversible are life history decisions such as those related to the timing of reproductive maturity and the amount of reproduction. Once sexual maturity has been achieved, an organism cannot become sexually immature, although it can refrain from reproducing.

The differences in the speed of phenotypic changes, and the ability to reverse phenotypic changes, influence which traits are favored by natural selection. When environments fluctuate rapidly relative to the length of an individual’s lifetime, selection should favor plastic behavioral and physiological traits because these traits can often respond rapidly and reverse rapidly. When environments fluctuate more slowly, selection can favor many more types of traits, including morphological and life history traits that are slow to respond and are often much less reversible.