Frozen Evolution. Or, that’s not the way it is, Mr. Darwin. A Farewell to Selfish Gene.

The name of the theory is frozen plasticity theory. However, the theory was described in great detail in a popular book entitled “Frozen Evolution”. It is quite probable that the correct name of the frozen plasticity theory will be replaced by the wrong name the frozen evolution theory due to memetic drive. 

The punctuated equilibrium model presented by Eldredge and Gould in the early seventies suggests that species usually evolve in a punctuated way – they develop their typical phenotype very quickly and for most of the time of their existence their phenotype remains stable or changes only very little. The theory of frozen plasticity 1) suggests a genetic mechanism for such an evolutionary stasis of species, 2) suggests a genetic and ecological mechanism of transition from a stable to a plastic state (different from all mechanisms suggested in the past thirty years by students of punctuated equilibrium, including Eldredge and Gould), and 3) suggests many nontrivial macroevolutionary, microevolutionary and ecological implications of the frozen plasticity theory.   

Only a negligible fraction of sexually reproducing species at a given time (the species originated recently, for example, by peripatric speciation) are plastic. Most species behave as elastic in microevolutionary processes and as frozen in macroevolutionary processes. They respond to a minor environmental change by reversible change (accompanied by a decrease in fitness) and to a major environmental change by extinction rather than by evolutionary adaptation. 

The first version of the theory of frozen plasticity was presented in the paper: On the "origin" of natural selection by means of speciation. Flegr J. 1998, Riv Biol -Biol Forum 91:291-304.

The frozen plasticity theory published in 1998 in Riv Biol -Biol Forum 91:291-304 is still valid in principle, however, not in all details. The major modification concerns the mechanism of the transition from an elastic to a plastic state. The original model suggests that most genetic polymorphism (the major obstacle to adaptive evolution in sexual species) disappears due to a drastic reduction of the population size during peripatric (or, e.g., chromosomal) speciation due to the bottleneck effect. The current version of the frozen plasticity theory assumes that the most important part of genetic polymorphism, i.e., the genes (more correctly the alleles) which are sustained in the population due to frequency-dependent selection, is eliminated in the second phase of speciation by genetic drift, i.e., when the new population balances on the edge of extinction for several generations.  

Not at all. In a certain sense, the frozen plasticity theory means a return to the Darwinian theory based on individual selection from the current mainstream theory which is based on intralocus competition of alleles (the selfish gene theory). The current theory of adaptive evolution (which silently replaced Darwin’s theory in the past thirty years) suggests that the new adaptive trait evolves because it helps to increase the number of copies of the allele that is responsible for the transmission of this particular trait to future generations. The frozen evolution theory suggests that both this mechanism and the old Darwinian mechanism, which is based on competition for higher fitness of an individual, can be responsible for the origin of an adaptive trait. However, the frozen plasticity theory suggests that both these mechanisms can operate only in the plastic phase of existence of a species.   

In a certain sense yes. Richard Dawkins proposed the theory to explain the evolution of adaptive traits in sexually reproducing organisms. He argues that the fitness of an organism is determined by its genotype, and the genotype (and therefore, also, the fitness) is not inherited from parents in sexually reproducing species but originates in every generation de novo by mixing half of the genes from one parent and half of the genes from the other parent. In contrast, the gene, defined by Dawkins as a small piece of DNA responsible for a particular trait, is regularly inherited from generation to generation in unchanged form even in sexual organisms. Therefore, the genes (in fact, the alleles) but not the individuals can be the subjects of biological evolution. The selfish gene theory is better than the original theory of intrapopulation individual selection, as it offers a unified theoretical framework for explaining a broader spectrum of evolutionary phenomena. It explains not only the evolution of adaptive traits but also the evolution and spread of certain alleles which decrease the fitness of their carrier (outlaw genes in Dawkins’s terminology), as well as the spread of a category of altruistic genes, i.e., alleles for behavior which decrease the direct fitness of their carrier while increasing its inclusive fitness by increasing the direct fitness of its relatives.

The frozen plasticity theory, however, shows that the selfish gene theory fails in its original objective, i.e., in explaining the mechanism of adaptive evolution in sexual organisms. It is true that the allele is regularly transmitted from generation to generation in an unchanged form. At the same time, the influence of an allele on a particular trait, as well as the influence of a particular trait on the fitness of an individual, is very often context dependent – in a particular genotype the same allele influences the trait negatively, whereas in another genotype the same allele influences the same trait positively. In the context of one phenotype the particular trait influences the biological fitness positively, while in the context of another phenotype the same trait influences the fitness negatively. Moreover, the influence of the particular trait on the fitness very often quantitatively or even qualitatively depends on the frequency of the trait in a population. Therefore, in sexual (genetically polymorphic) species neither the Darwinian nor the Dawkinsonian mechanism can explain the evolution of adaptive traits.
 

The frozen plasticity theory was developed to explain the evolution of adaptive traits in sexual species. The phenomenon of frequency-dependent selection plays a very important role in the resistance of a genetically polymorphic population to adaptive evolution in sexual organisms where in every generation the alleles of two parents meet each other in new zygotes. The selective value of an allele depends, for example, on the probability that the same allele is present in the chromosomes of both paternal and maternal origin, which depends on the frequency of the allele in the population. This source of frequency dependence of the selective value of alleles does not exist in asexual organisms; however, some sources of frequency dependence are present even here. Frequency dependence could take part in ecological interactions between host and parasite. A parasite is often specialized for exploitation of the most common form of its host, for example, a host with the most common MHC alleles. Similarly, the immune system of a host is usually adapted to the most common strain of a parasite. An asexual species can be a mixture of phenotypically and genetically different strains with differing strategies to exploit resources from their environment. The frequencies of particular strains could change in response to changes in the environment: They will probably express a tendency to return to some state of equilibrium. The long-term competition of strains with selective values dependent on their frequency in the population could be an important source of species cohesion and resistance of the population to adaptive evolution even in asexual species.  

The frozen plasticity theory can explain a broader spectrum of biological phenomena than the earlier theories by Darwin and Dawkins. The frozen plasticity theory suggests that a certain rather probable hypothesis on the nature of evolutionary stasis (frequency-dependent selection and pleiotropy-based elasticity of genetically polymorphic species) and evolutionary plasticity (loss of genetic polymorphism due to the founder effect during peripatric speciation, and drift following it) could have a very important impact, not only on macroevolutionary but also microevolutionary and ecological processes. In fact, the picture of evolutionary and ecological processes presented by the frozen plasticity theory differs in many respects from that provided by the current textbook theory of evolution. Most of these predictions could be tested empirically and should be analyzed in greater depth theoretically. In my opinion, the frozen plasticity theory, which includes the Darwinian model of evolution as a special case - the evolution of species in a plastic state - not only offers plenty of new predictions to be tested, but also provides explanations for a much broader spectrum of known biological phenomena than classic evolutionary theories. 

Some important differences in predictions of the nature of microevolutionary, macroevolutionary and ecological processes are given in the following table:

As shown by T.S. Kuhn, in contrast to simple scientific hypotheses, complex scientific theories can be neither verified nor falsified. A new scientific theory usually outcompetes the old theory because it is more elegant and more simple. Later on, it often turns out that the new theory covers a broader spectrum of biological phenomena than the old theory; however, this is not the main reason for its victory. The usual mechanism of the victory of a new theory is generation turnover. The book “Frozen Evolution” says: „Until the old proponents and co-creators of the original Neodarwinist theory leave for a better world or at least for a welldeserved rest, and are replaced by a new generation of scientists that, metaphorically speaking, absorbed the selfish gene theory with their mother’s milk, and until these scientists decline sufficiently to start writing their own textbooks, the new theory will be presented in textbooks maximally as a sort of cream on the cake and not as the basic theoretical framework of the field.“

According to the theory of frozen plasticity, representatives of the old, macroevolutionarily frozen, microevolutionarily elastic species that are kept out of their original state by natural selection, have lowered fitness (viability or fertility) in comparison with representatives of young species living under conditions similar to those existing at the time of their origin. Therefore, statistically, the population density of a species probably negatively correlates with species age; a study of the correlation of the molecular age of species with their average abundance could easily test this prediction. This could also explain the existence of the most universal ecological law – that every community shows a concave curve on a histogram with many rare species and just a few common species. The position of a species on the histogram is rather stable; species retain their basic status as common or rare for as long as one million years. The frozen plasticity theory predicts that the common species are the young species which are still evolutionarily plastic or which have only recently lost their plasticity and are therefore still adapted to current environmental conditions.
 

According to classical evolutionary theories, native species, which are adapted to local conditions, should outcompete newcoming species. According to the frozen plasticity theory, the ecological success of some newcomers is not so surprising. During the introduction and following lag phase, the genetic polymorphism of an introduced population decreases, which could result in the conversion of a frozen species to the plastic state. Frozen species are best adapted to the conditions existing at the time of their origin (past conditions), while plastic species can adapt to current conditions. Moreover, plastic species can outcompete frozen species in the coevolutionary “arms race”.

The existence of only a low fraction of evolutionarily plastic species can also explain the fact that man succeeded in domesticating only a negligible number of plant and animal species. Only plastic species can adapt to the drastically changed conditions of life in captivity without significant decreases in viability and fertility. The frozen plasticity theory suggests that domestication should be successful mostly in young species, which have not yet had enough time to freeze.

The plasticity of asexually reproducing species should be better off in an environment, in habitats poor in resources or where the survival of most species is limited over a long period of time by unfavorable abiotic factors. Here, the main criterion of evolutionary success is how well (not how quickly) the species can change its phenotype in response to the requirements of the environment. It is noteworthy that asexually reproducing species or asexually reproducing lineages of otherwise sexually reproducing species of plants and animals are found primarily in habitats with extreme conditions – in habitats which are extremely dry, extremely cold or extremely poisonous. The proportion of asexual species increases, for example, with increasing altitude and latitude or in places where the soil contains high concentrations of toxic heavy metals. On the other hand, sexually reproducing (elastic) species should be better off in an environment rich in resources and with many competing species where the rate of evolutionary responses in the coevolutionary “arms race” plays the crucial role. The fact that they can retain most of their genetic polymorphism enables them to rapidly respond to any evolutionary pressure by shifting the frequencies of their alleles, without needing to wait for rare, advantageous mutations.

Evolutionary elasticity of sexual species could also be advantageous in a long-term perspective. Under fluctuating conditions of a stochastic environment, a plastic asexual species can adapt to a transient environmental change, while an elastic sexual species resists such change of its phenotype. When the environmental conditions return to normal, the plastic species can fail to return to its optimal phenotype quickly enough, and is therefore at risk of extinction, while the population of an elastic species is able to return to its original phenotype within a few generations. As was already suggested by G.C. Williams, the main advantage provided by sexual reproduction may consist in a substantial reduction in the evolutionary ability of most species. As a consequence of their elasticity, sexually reproducing species are evolutionarily passive throughout much of their existence and cannot opportunistically (i.e., without regard to future negative consequences) respond to temporary short-term changes in external conditions.

According to classical evolutionary theories, there should be no correlation between cladogenesis and anagenesis (between speciation and changes in the phenotype of organisms), while the frozen plasticity theory assumes that the irreversible phenotypic changes are always associated with speciation. The frozen plasticity theory predicts that the number of evolutionary changes in a phylogenetic lineage reflects the number of speciations in this line rather than its age. These two parameters often correlate with each other; however, modern multivariate statistical techniques allow testing the effects of these two parameters separately. A study in passerine birds has found the number of speciations within a phylogenetic line to have a very strong positive effect on the rate of anagenesis. The number of species alone explained 33.3% of the total variation in morphology. A positive correlation between the rates of anagenesis and speciation can be detected even on the molecular level. A molecular study has shown that a relatively large part of the variability in the substitution rate can be explained by differences in the speciation rate between evolutionary lineages.

The theory of frozen plasticity suggests that important changes in the phenotype (e.g., morphology) of species occurs only in evolutionarily plastic species, i.e., those species which originated by peripatric speciation (for example, by colonization of an oceanic island) rather than by allopatric speciation (for example, by splitting the original geographic area of a species into two parts of similar size by a new geographic barrier). Biogeographical data suggest that the rate of anagenesis on islands is really higher than on the mainland. Also, many taxa, the most „strange“ species, usually occur on oceanic islands rather than on the mainland. The higher frequency of peripatric speciation on islands than on the mainland can be the clue to the observed phenomena.

The frozen plasticity theory also offers a new explanation for the existence of evolutionary trends, the slow directional phenotypic changes in organisms of particular phylogenetic lineages which endure much longer than the individual species involved. The main problem with the existence of such trends is that they are too slow to be geared by natural selection. The change in the value of the trait per generation is so small that it is absolutely invisible for natural selection. According to classical evolutionary theories, the selection pressure has to be strong enough to overpower the effect of genetic drift. However, such selection should result in far more rapid evolutionary changes than those which come to light as evolutionary trends in the paleontological record. The frozen plasticity theory suggests a new solution to the problem of very slow evolutionary trends. According to this theory, the trend could in fact be a product of a relatively strong and long-term selective pressure to which species can respond, however, only in short and rare periods of their evolutionary plasticity.

Phylogenetic trees are usually shrub-shaped rather than tree-shaped. Most disparate species originate at the same time and possibly from a common ancestor as a result of the process of adaptive radiation. Particular species, which have originated in a common radiation event and from a single evolutionarily plastic ancestor, coexist for a long time without splitting off new species. Most branches end without producing a successor; however, some of them could split off a new plastic species which could undergo a new burst of radiation. Interestingly, such a tree is similar in shape to the figure drawn by Charles Darwin and unlike modern trees (which are usually automatically interpreted as phylogenetic trees but in fact are inspired by the shape of the cladogram, a graphic representation of the distribution of synapomorphies within a studied taxon).

Both phenomena (higher variability of early-branched species and decreasing speciation rate of clades) could have a common cause, namely, the continuous irreversible freezing of more and more traits during the evolution of a clade. It is certain that the traits differ in resistance to transition from frozen to plastic in response to reduction of genetic polymorphism. This process is likely to occur readily for some traits and can be achieved by a relatively small reduction in genetic polymorphism. For other traits, the transition from frozen to plastic is difficult or even impossible, as it requires an unrealistically small founding population and an unrealistically long period of persistence of such a small population in an extinction-prone state. On a macroevolutionary time scale, more and more traits pass into the permanently frozen state due to the universal process of sorting on the basis of stability. The stable traits (and systems and such) persist, while the unstable traits (and systems and such) pass away. In a new clade, a high proportion of species contains many traits which could melt during standard peripatric speciation or which are relatively plastic even on the level of a species (or even of a local population). Through time, more and more traits in more and more species turn into a semipermanently or even permanently frozen state. The representatives of a particular clade are not only less and less variable (more and more elastic – resistant to selection pressure), but also exhibit elasticity that is less and less affected by peripatric speciation. Originally, many representatives of a clade had the capacity to evolve new body plans after peripatric speciation. In the end, only some species retain this capacity, and even in these species some traits have a highly limited capacity to respond to selection after peripatric speciation.

The Cambrian explosion is the rapid origination of probably all extant (and also many other already extinct) metazoan phyla around 545 million years ago. All of the basic architectures of animals were apparently established by the end of the Cambrian explosion; subsequent evolutionary changes, even those which allowed animals to move out of the sea onto land, involved only modifications of those basic body plans. Most probably, not only the general diversity of metazoan body plans, but also the diversity within particular phyla, reached its maximum within 10-15 million years of the Cambrian, and decreased throughout the following 500 million years. The existence of the Cambrian explosion is in accordance with the predictions of the frozen plasticity theory. At the beginning of the evolution of the metazoan clade, many traits, even those which determine the basic architecture of animal body plans, had the capacity to become plastic during peripatric speciations in many metazoan lineages. For an explanation, see also the question: “Why does the variability of species decrease with the age of the phylogenetic line and why does the maximal diversity (more correctly, the maximal disparity) of phylogenetic lines occur early in the history of the lines”. Therefore, a rather radical remodeling of body architecture as well as the origin of new body plans in response to particular selection pressures, were possible in the early stages of metazoan evolution. Through time, more and more traits came to be permanently frozen. Most probably, different traits would lose the capacity to turn plastic in differing successions in particular phyla. Therefore, anagenetic potential faded, and adaptation to new environmental conditions came to be based on modification of existing body plans rather than on building new ones.

The theory of frozen plasticity suggests that the taxonomic category of species, and even more that of genus, could objectively denote the existing entity, rather than a merely useful epistemological construct of biologists. Within the theory of frozen plasticity, a biological species can be defined as a set of individuals sharing an identical gene pool throughout the period between two speciating events. Similarly, a genus can be defined as a set of individuals sharing a common exclusive ancestor in the time between two periods of evolutionary plasticity.

In fact, the frozen plasticity claims that sexual species are not microevolutionary frozen but elastic. Therefore, they readily respond to selection at first (actually, more readily than microevolutionary plastic asexual species), however, they stop responding after the frequencies of alleles decline enough from their equilibrium state. The human races declined from their original state so quickly because of their microevolutionary elasticity.