The capacity of an organism of a single genotype to generate two or more phenotypes by alternative developmental paths is an example of the adaptive norm of animals to which Schmalhausen drew attention. Developmental plasticities differ from physiological adaptations in that after a critical time in the animal's development they are irreversible. The alternative phenotypes can be distinguished by their morphology, physiology, or behavior. Organisms with alternative phenotypes are called polyphenic.
There are two principal kinds of polyphenism, sequential and alternative. Taking sequential phenotypes first, the cases include animals with complex life cycles of two or more different developmental stages (such as larva, juvenile, and adult). Most animal phyla inhabit the ocean, and most pass through strikingly different developmental stages. The larva might feed in the plankton-rich surface layer of the ocean, whereas the adult might live in the mud, sand, and rocks near the shore. In the case of ascidians (sea squirts), the larval and adult forms look so different that they were thought to be members of different phyla until the late 1800s, when the development of the larva to the adult was followed. Some parasitic flatworms (trematodes) have five or six successive forms, each highly specialized for different lifestyles in different hosts. Of course, for terrestrial animals, we are familiar with the vegetarian wall-eyed swimming tadpole as the amphibian larval phenotype and the carnivorous four-legged frog as the adult pheno-type—or the wingless, legless caterpillar and the adult butterfly.
When stages of a life cycle differ dramatically, they are connected by a drastic metamorphosis. In the metamorphosing caterpillar, most larval tissues are destroyed and replaced by newly developed adult cells. The transition from one stage to the next is usually dependent on external conditions, although it must be appreciated that this dependence is evolved and selected. Two hormones control insect metamorphosis: ecdysone, a steroid-like hormone, and juvenile hormone, a close relative of vitamin A. Though made by the insect, their times of synthesis and effectiveness are subject to aspects of nutrition, light, and temperature.
Unlike hormones, such as insulin, which are involved in maintaining a stable internal environment ecdysone and juvenile hormone do not maintain the original state; rather they globally release the internal means to propel the organism to a new state. In butterflies, there are specific times in the last larval period when the full-grown caterpillar responds to juvenile hormone by turning off genes appropriate for the larva and turning on genes appropriate for the pupa. These effects, though far-ranging, are mechanistically no different than the common process of gene regulation that occurs in all cells of our body. The timing of the response to juvenile hormone is itself regulated by periodic pulses of ecdysone. Different tissues respond differently to juvenile hormone and ecdysone, various cells responding to one or the other, both, or neither. Where there has been a response to external conditions, it is the organism that specifies the response, the readiness to respond, and the specificity for responding to a particular environmental agent. Thus, the same genome can be read differently at different times to drastically alter the phenotype. The timing of these events can be linked to the external environment or can be driven by purely internal means.
Sequential phenotypes have in some cases provided the pheno-typic variety for the founding of new races or species. Salamander species exist in which the "adult" is basically a large larva that has gained sexual maturity. It retains larval traits such as a finned swimming tail, large external gills, and an aquatic lifestyle. Metamorphosis from the larva to adult, which is normally thyroid hormone dependent, is largely forgone.
The lake-dwelling axolotl of the Mexican highlands is a well-
known example. When thyroid hormone is experimentally provided, the animal completes metamorphosis and comes to resemble a related land-dwelling species (of Texas). Plausibly, the axolotl is derived from a metamorphosing ancestor, in which sexual development was prematurely completed in the larva and thyroid hormone production was lost by a heritable defect. It has been argued that the Mexican highlands are cool and deficient in iodide, two conditions known to hinder or block metamorphosis. The axolotl may have overcome the conditions by omitting metamorphosis altogether. Its apparent morphological novelty as an adult is the retention of larval features already present in the ancestor, not the origination of new features. This kind of persistence of the juvenile form is common in salamanders.
In another case, the landlocked salmon of freshwater lakes is thought to be an arrested alternative phenotype of an ancestor that moved between saltwater feeding grounds and freshwater spawning grounds. The landlocked adult resembles a "parr" form of salmon, which is a dark, bottom-dwelling juvenile that in the ancestor would have undergone a thyroid-hormone-triggered metamorphosis to a silvery migratory adult.
Whereas these examples involve the retention of larval or juvenile traits, other cases involve the loss of the larval stage and a direct development of the embryo to the adult. In sea urchins, most species produce small eggs that develop to bilateral plankton-feeding larvae that, after much growth, metamorphose to a penta-radial adult, a radical transformation of body organization. In every family of sea urchins are species that have evolved a direct form of development that omits the larval stage. Their eggs are larger and contain more yolk. The large embryo develops directly into a small adult. The larval feeding stage has been omitted, and the bilateral development of the embryo has been modified—nearly skipped—to yield directly a penta-radial outcome. If one unknowingly compared what hatched from the eggs of closely related direct and indirect developing species, one would say the difference is enormous; but in fact the one species represents only an omission of part of the adaptive norm of reaction of the other. Little evolutionary novelty is involved. Novelty has been generated, but it has been generated by omission rather than by creating new processes.
In some ways the more interesting forms of developmental plasticity occur when the organism has alternative adult phenotypes developed in accordance with environmental or social conditions, the second kind of polyphenism. The irreversibility of this polyphenism is due to an environmentally dependent branch point, controlled by a sensitive switch, at one episode of development. When this decision has been made, it cannot be repeated or undone.
Social insects such as ants, wasps, bees, and termites offer dramatic examples of alternative adult phenotypes. Honeybees are a favorite experimental model of phenotypic plasticity. When the dominant queen emerges from the pupa slightly ahead of contending queens, she takes over the nest. The older mother queen leaves, taking a host of worker bees with her. These are her sterile diploid sisters, sharing three quarters of her genetic information. The fertile queen and sterile workers are obviously alternative phenotypes of the same genotype.
Compared to the workers, the queen is larger but has smaller eyes, reduced mouthparts, shorter antennae, a smaller brain, no pollen-collecting combs, rakes, or baskets on the leg, and poorly developed glands of the sort used by workers to build the waxy hive and to feed larvae with royal jelly or worker jelly (illustrated in Figure 13). However, the queen develops very large ovaries and specialized glands producing "queen substance," which controls the behavior of the workers. The queen is the reproductive alternative phenotype, fed by the workers and producing over a thousand eggs a day. She is figuratively the germ line of the colony. The workers, who are sterile because their ovaries remain undeveloped, collect food, do the waggle dance to inform other workers of the location of flowers, deposit honey, build the cells of the hive, supervise the deposition of eggs, feed the larvae and nurse workers, and air-condition and clean the hive. They are the soma of the colony. Clearly, the queen and the worker are very different phenotypes.
How do they develop one way or the other? Both come from the same kind of diploid egg at the start, as shown by experiments trans-
ferring eggs between royal cells and worker cells—whatever egg is in the royal cell becomes a queen. Workers construct royal cells at a time when the queen mother produces insufficient queen substance to inhibit them from doing so, and the workers start preparing royal jelly and feeding it to larvae in these cells. Royal jelly is a nutritious substance, which in honeybees includes high concentrations of vitello-genin, a protein found in both vertebrate and invertebrate egg yolk. By the third day of larval life, the prospective queen differs from the prospective worker in its development, as shown by the fact that a change of diet to worker jelly or a change to a worker cell no longer alters the outcome. Queens develop faster and emerge from the pupa after only 16 days, whereas workers emerge at 21 days. The first queen out may kill her tardy sister queens and take over the hive (the mother queen has already left), or she may leave in a swarm.
It is during the larval period that the choice is made to develop to either the worker or the queen. Strong evidence exists that royal jelly and worker jelly differ in controlling the level ofa hormone needed during the brief time of larval development to the queen. Royal jelly raises the level of juvenile hormone during this critical period; in fact, topical application of juvenile hormone can induce the formation of a queen. Research is just beginning on how the larva responds to the royal and worker jellies to generate the different morphs. It is known that several genes are differently expressed in the worker and the queen. Workers, though smaller, are in fact more complex in their anatomy and physiology than queens, which are basically egg-producing factories with many rudimentary body parts.10
Polyphenism is not limited to insects. A predatory species of cichlid fish (Cichlasoma managuensa) can develop either blunt jaws for biting prey or pointed jaws for sucking in prey. If newly hatched fish are raised in the laboratory under two feeding conditions, their jaw development is different. The young start with small, blunt jaws; if they feed on flake food for 16.5 months, they develop into adults with full-sized, blunt jaws. If they instead feed on brine shrimp for the same period, they develop into adults with large pointed jaws. The difference in jaw structure is apparent by 8.5 months. If the blunt-
jawed fish eating flake food are switched to brine shrimp at this time, they can still develop pointed jaws, but if switched soon thereafter, they cannot. Jawbone development before 8.5 months probably responds to the dynamic load of feeding.11
Cichlid fish, as a worldwide group, are unusual in having a second set of jaws in the back of the mouth: the pharyngeal jaws, shaped from a throat bone. The availability of two jaws has allowed a division of usage, the front pair for ingesting the food and the second pair for chewing it. Humans, on the other hand, demand both functions from one pair of jaws, and each function probably limits the specialization of the other. This plasticity of development concerns the front jaw of this particular species of cichlid. In another, the development of the back jaw also shows developmental plasticity. It becomes wider and fills with crushing teeth when the diet is rich in mollusks rather than insects.
Overall, the phenotypic plasticity of jaws and the presence of independently specialized jaws in cichlids may explain their position as one of the most species-rich groups of animals, with as many as five hundred species in just one African lake. Some of these species are thought to have arisen by the mutational stabilization of one or the other alternative phenotype of an ancestor possessing rich developmental adaptability.12
Plasticity and fixation may underlie much evolutionary change. The different developmental alternative phenotypes of an organism's complex life cycle, and the alternative adult phenotypes, are aspects of the total phenotypic plasticity of the organism (the whole adaptive norm of reaction of Schmalhausen). Evolutionary specializations, made heritable by new genetic variation, are but stabilizations of certain already-available states, in the mode envisioned by Baldwin, Schmalhausen, Waddington, and West-Eberhard.13
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