Phenotypic variation in leaf form in the semiaquatic plant Ranunculus aqu atilis. Compare the filamentlike leaves on submersed branches (a) with normally structured leaves on branches above the water (b).

The phenotype consists not only of the structure of an organism and of its physiology, but also of all the products of the behavioral genes. This includes the nest a bird builds, or the web of a spider, or the path of migration of a migratory bird. Dawkins (1982) has referred to these aspects of the characteristics of an organism as the extended phenotype. It is as much (and often more so) the target of selection as the structural characteristics of an organism.

The range of phenotypic variation that a particular genotype is able to produce is referred to as its norm of reaction. Thus the phenotype is the result of the interaction between genotype and environment. Some species have a very wide reaction norm; they can adjust their phenotype to wide variations of the environment and have a high phenotypic plasticity. The fact that it is the phenotype, rather than the genotype, that is the target of selection allows the existence of considerable genetic variation in a gene pool. Such variation is compatible with selection as long as the produced phenotypes have an acceptable selective value.

Because the phenotype is the product of the genotype, it has both evolutionary stability and evolvability. Many core processes at the cellular level are conserved throughout the metazoa, such as many signaling pathways and genetic regulatory circuits, others are conserved throughout the eukaryotes (e.g., the cytoskeleton), and yet others throughout all life-forms such as metabolism and replication. Sequence conservation is so strong that more than half of the coding sequences of yeast are recognizable in mice and humans. The actins of yeast and humans, for example, are 91 percent identical.

These core processes, however, must not be so structured that they prevent further evolution. Indeed there is ongoing selection for evolvability of the phenotype. Only this flexibility permits the occupation of new adaptive zones and the successful coping with new environmental challenges. The study of the properties of a genotype that allow it to cope with the constraints of the conserved portions and to maintain optimal evolvability is one of the frontiers of current evolutionary biology.

OTHER POTENTIAL OBJECTS OF SELECTION

The individual is not the only entity that has been suggested by one or another evolutionist to be the object of natural selection. We have already refuted this claim for the gene, and will now discuss gametes, groups, species, higher taxa, and clades.

Gamete Selection

All gametes are subject to selection between the completion of the meiotic cycle and either fertilization or death. Elimination is extremely severe since only a very small fraction of the gametes is successful. Unfortunately, we know very little about the eliminating factors. Experiments have revealed that the proteins of the egg wall in certain marine invertebrates have the capacity to prevent the entry of some spermatozoa while admitting others. What fitness criteria are involved here is still unknown. The properties responsible for gametic selection are important isolating mechanisms, referred to as gametic incompatibility.

Gamete interaction has been studied much more intensively in plants, particularly the compatibility reactions between pollen tubes and the stigma or style. In many taxa, special mechanisms prevent self-pollination. Less is known about incompatibilities among out-crossing species and how it is controlled. As early as the 1760s the botanist J. G. Kölreuter showed that when conspecific and alien pollen were placed on the stigma simultaneously, it was always the conspecific pollen that fertilized the seed. If the alien pollen alone was placed, it successfully fertilized in some species pairs.

Group Selection

There has been much argument whether a group of individuals can or cannot be the object of selection. The situation is clarified if one makes a distinction between “soft” and “hard” group selection (Mayr 1986). Soft group selection refers to selection of casual groups, and hard group selection to cohesive social groups. In the case of soft group selection, the fitness of the group is the arithmetic mean of the fitness values of the members of the group. This mean value has no effect whatsoever on the fitness of the composing individuals. The evolutionary success or failure of such a group (“group selection”) is simply the automatic consequence of the fitness of the composing individuals. The fact that they are associated in a group makes no contribution to their fitness. Such soft group selection makes no independent contribution to evolution. This is the kind of “group selection” one finds in casual groups. Soft group selection really should not be referred to as group selection, because the group as such is not selected. A population as a whole is subject to such soft “group selection.”

However, in certain species a special kind of group occurs, social groups, that can indeed be a target of selection. Such a group, owing to social cooperation among its members, has a greater fitness value than the arithmetic mean of the fitness values of its individual members. This may be called hard group selection. Members of such groups cooperate by warning of enemies, sharing newly discovered sources of food, and joint defense against enemies. This cooperative behavior enhances the survival propensity of such a group. The human species, at least during the hunter-gatherer stage, benefited from such social cooperation and this led to increased survival of certain groups. As a result, any genetic contribution toward cooperative behavior would be favored by natural selection. It is believed that this social cooperation has been an important factor in the development of human ethics (see Chapter 11). Hard group selection does not replace individual natural selection, but is superimposed on it.

Kin Selection

A form of selection called kin selection is recognized by many evolutionists, particularly in connection with the evolution of altruism. It is defined as selection for characteristics that favor the survival of close relatives of a given individual who shares part of the same genotype (known as inclusive fitness altruism). Except for parental care and in social insects, kin selection is probably not as important a factor in evolution as sometimes believed, particularly when there is a considerable exchange of individuals among neighboring groups. The altruism that members of a social group show to other related members of the group (excluding offspring) is apparently never anywhere near as great as the altruism displayed by parents (particularly mothers) to their own offspring. It is perhaps misleading to combine the two kinds of relationship under the single term kin selection. However, since members of a social group are often closely related to each other, much hard group selection is simultaneously kin selection. (See also Chapter 11.)

Species Selection

The history of evolution is a steady extinction of species and the origin of new species. This turnover is often apparently due to the superiority of a new species over an established species. Also, when species of different biota come into competition, as did those of North and South America after the isthmus of Panama had been established in the Pliocene, it can result in considerable extinction, part of it caused by competition between the invaders and the indigenous species. This phenomenon has been called species selection. As mentioned earlier, Darwin called attention to the frequent extinction of native species of plants and animals on New Zealand after European species had been introduced. The mistake was made by some authors to consider this an alternative to individual selection. In reality, this so-called species selection is superimposed on individual selection. The individuals of both species coexist after the entry in the same niche, and extinction takes place when the individuals of the invading species are, on average, superior to those of the indigenous species. Clearly, it is a selection of individuals. Misunderstandings are avoided if this process is called “species turnover” rather than “species selection” (see Chapter 10). A species as a unit is never the object of selection, only its individuals.

An even higher taxonomic level is involved in so-called clade selection, a clade being a holophyletic group of taxa forming a branch of a phylogenetic tree. Owing to the Alvarez extinction event at the end of the Cretaceous, the clade of the dinosaurs became extinct, but not the clades of birds and mammals. During every mass extinction certain higher taxa have fared better than others. Again, the actual objects of selection were individuals, but the individuals of some clades shared characteristics that favored survival through the extinction event, while these characteristics were absent in the individuals of the losing clades. What is remarkable for mass extinctions is that a whole higher taxon may be eliminated almost instantaneously or at least during a relatively short period. Clade extinctions also sometimes occur that are not clearly the result of a mass extinction. The extinction of the trilobites may be an example.

Competition Among Higher Taxa

Mass extinctions have called attention to the possible competition between higher taxa. Mammals had existed for some 100 million years prior to the mass extinction at the end of the Cretaceous, but they were small, insignificant, and quite likely nocturnal. Why did they enjoy such an explosive radiation in the ensuing period of the early Tertiary? The most widely accepted answer to this question is that they were able to enter all the ecological niches vacated by the demise of the previously dominant dinosaurs. Evidently the two classes of animals had been competing all along, but the dinosaurs had been superior competitors. Obviously, the mammals did not cause the extinction of the dinosaurs, but they replaced them when the dinosaurs became extinct owing to a nonbiological cause.

This case of the mammalian flourishing also illustrates the phenomenon of explosive speciation in previously vacant niches. Other examples are the species flocks of fish, molluscs, and crustaceans in ancient lakes and the rapid radiation of colonists of oceanic archipelagos. There are more than 700 species of drosophilid flies and over 200 species of crickets on the Hawaiian Islands. The honey creepers (Drepanididae) in the Hawaiian Islands and the geospizid finches in the Galapagos are other well-known cases of such radiation.

In all of these cases it was the absence or the removal of competition that made the radiation possible. One speaks of displacement when an incumbent taxon is exterminated by competitive exclusion owing to the arrival of a superior competitor. To actually prove the causal connection in such a sequence is difficult. For instance, the multituberculates were a flourishing group of nonplacental mammals in North America in the late Cretaceous and Paleocene. But when, in the Eocene, the first rodents appeared (probably from Asia) and became extremely successful, common, and widespread, the multituberculates became rare and finally died out. The extinction of the trilobites when the bivalves became so successful is another possible case, but an environmental catastrophe has also been proposed for their demise. Throughout the history of paleontology there are numerous similar cases of the sudden decline and ultimate extinction of a previously prosperous taxon after a new taxon with seemingly similar ecological requirements had appeared. It is, of course, impossible to prove in any of these cases that it was the arrival of the new competitor that caused the extinction, but this scenario often fits the known facts better than any other explanation.

WHY IS EVOLUTION USUALLY SO SLOW?

When the pharaohs’ tombs were opened in Egypt early in the nineteenth century, not only human mummies were found but also those of sacred animals such as cats and ibises. When the anatomy of these animal mummies, estimated to be about 4000 years old, was carefully compared by zoologists with living representatives of these species, no visible differences could be found. This finding was in striking contrast to the rapidity with which animal breeders had produced pronounced changes in domestic animals in a much shorter time. Consequently, the absence of any visible change in these mummies was used as an argument against Lamarck’s theory of evolution. Now we know that it usually takes many thousands if not millions of years for visible changes in evolving species to occur, except in a few special situations. Hence, the constancy of the Egyptian mummies is no evidence against evolution.

With drastic selection taking place in every generation, it is legitimate to ask why evolution is normally so slow. The major reason is that owing to the hundreds or thousands of generations that have undergone preceding selection, a natural population will be close to the optimal genotype. The selection to which such a population has been exposed is normalizing or stabilizing selection. This selection eliminates all of those individuals of a population who deviate from the optimal phenotype. Such culling drastically reduces the variance in every generation. And unless there has been a major change in the environment, the optimal phenotype is most likely that of the immediately preceding generations. All the mutations of which this genotype is capable and that could lead to an improvement of this standard phenotype have already been incorporated in previous generations. Other mutations are apt to lead to a deterioration and these will be eliminated by normalizing selection. There are also some special genetic mechanisms, such as genetic homeostasis (including heterozygote superiority), that favor maintenance of the steady state.

FOUNDER POPULATIONS

The genotype is a carefully balanced system owing to the epistatic interaction of the composing genes. Selection for the replacement of a gene by a new one may therefore require adjustments at other gene loci. The larger a population, the slower will be the incorporation and spread of new genes. By contrast, a small founder population established by the offspring of a single fertilized female or by a few founders may be able to shift more quickly to a new adaptive phenotype since it is unconstrained by the cohesive forces of a large gene pool.

There is much observational evidence that evolutionary change to the level of completed speciation proceeds more rapidly in peripheral populations than in large widespread species (Mayr and Diamond 2001). The explanation for this is still controversial. Dobzhansky and Pavlovsky (1957) (Fig. 6.4) showed a long time ago that a group of small, originally identical populations diverged from each other much more rapidly than a group of identical large populations. Other laboratory studies of founder populations did not find a drastic change in such populations. However, most of the studies were made with Drosophila melanogaster, a species with a phenotype that is apparently particularly stable as indicated by its various sibling species. This constancy of D. melanogaster raises the possibility that different founder populations may react differently to their isolation. Traditionally, the greater evolutionary inertia of large populations was ascribed to the greater amount of pleiotropy and polygeny. However, another cause is presumably the distribution of different regulatory genes. Conservative gene flow does not reach isolated populations and interfere with their increasing divergence. There is every reason to believe that new discoveries in developmental genetics will contribute a better understanding of the causes for different rates of evolutionary change in general and in speciation in particular.

WHAT IS THE EVOLUTIONARY ROLE OF BEHAVIOR?

For Lamarck, behavior was an important cause for evolutionary change. He thought that changes in organisms caused by any kind of activity would be transmitted to future generations by the inheritance of acquired characters. For example, when giraffes stretched their neck to reach higher leaves, the resulting elongation of the neck would be inherited by the next generation. Even though this theory of inheritance is now refuted, evolutionists still believe, but for very different reasons, that behavior is important in evolution. A change in behavior, for instance, adoption of a new food item or increased dispersal, is apt to set up new selection pressures, and these may then lead to evolutionary changes (Mayr 1974). There are reasons to believe that behavioral shifts have been involved in most evolutionary innovations, hence the saying “behavior is the pacemaker of evolution.” Any behavior that turns out to be of evolutionary significance is likely to be reinforced by the selection of genetic determinants for such behavior (known as the Baldwin effect).

FIGURE 6.4

Variation, epistatic effects, and population size. The frequency (percent, vertical scales) of PP chromosomes in twenty replicate experimental populations of mixed geographic origin (Texas to California). The populations that have gone through a bottleneck of small population size show far greater variance after 17 months than the continuously large populations.

Source: Mayr, E. Animal Species and Evolution. Belknap (HU Press), 1966.