Flegr J. 1998: On the „Origin“ of natural selection by means of speciation. Riv.Biol./B. Forum 91: 291-304. The most important paper. It suggests a new genetic mechanism of evolutionary stasis and evolutionary plasticity.
Dep.Parasitology, Faculty of Science, Charles University, Vinicna 7, Prague 128 44, Czech Republic, E-mail email@example.com
Running title: Natural selection and speciation
Key words: Evolution, selection, heritability, fitness, punctuated equilibrium.
Abstract. A new model of evolution of adaptive traits in sexual species is suggested. As the expression of most phenetic traits is codetermined by many genes and the influence of a gene on the phenotypic trait is often gene-context specific, the heritability of phenetic traits in outbreeding populations is often low. Also the effect of expression of a single trait on biological fitness is often context specific being determined by the presence and level of expression of other phenetic traits. Because of the low heritability of phenetic traits and of biological fitness the potential for adaptive evolutionary change by means of natural selection is very limited in sexual species. However, most mechanisms of speciation lead to drastic reduction of genetic variance in the new species. In the absence of genetic variance genetic context for a new mutation is always the same and the heritability of phenetic traits and of biological fitness increases. After a renewing of genetic variance by mutation processes the heritability of traits and fitness again decreases. In the history of any sexual species a transient period of evolutionary plasticity in which the species can respond to natural selection and evolve new phenetic traits is followed by a long period of evolutionary stasis in which the species accumulates changes mostly by genetic drift and molecular or meiotic drive.
In Charles Darwin‘s time this model represented a beautiful hypothesis deduced on the basis of analogy with artificial selection of varieties of domestic animals and cultivated plants and possibly also with competition between economical subjects of developing industrial society. Today the Darwinian model is generally accepted in the whole scientific community. Most of the processes playing role in it were studied into deepest details and their molecular nature was revealed. We understand the mechanisms of storage and transfer of genetic information as well as the processes of the origin of new mutations. On the basis of both an elementary thinking and sophisticated mathematical analyses it seems evident that any systems functioning on the same principles as the biological systems do cannot but evolve.
When a phenetic trait is determined not by a single gene but rather by many genes of small effect then the inheritance of the trait must be not only blending but also vanishing. The descendant of two outcrossing individuals has only 50% genes identical-by-descent with its parent. Therefore the mutation that is beneficial for the parent occurs in a drastically new genetic context and the probability of it having an identical effect here as in the original context is highly reduced. In the next generation, the proportion of identical-by-descent genes decreases down to 25% and similarly decreases also the chance for identical phenotypical effect of the mutation. Within a few generations the unique combination of genes, which determine the unique phenetic trait, is outdiluted and the unique trait can disappear from the population. The mutation, which was responsible for the original occurrence of the trait, however, still persists there and can reveal its presence whenever it occurs in the genomes of possibly rather unrelated individuals with proper combination of alleles in their genomes.
Accepting the facts that because of the genetic context sensitivity of a gene effect the hereditability of phenetic trait is low, and that because of whole-phenotype context sensitivity of effect of the phenetic trait on the organism‘s fitness the hereditability of fitness is very low, if any, we have to abandon the classical model of neodarwinian evolution in sexual organisms. To allow the fixation of a context sensitive trait in an outcrossing population by means of natural selection its effect on the fitness would need to be unrealistically high. Natural selection can fix an unconditionally beneficial trait coded by a single gene or by a few genes with strictly additive effects. It is not clear what role such genes of major effects can play in biological evolution. The mutations with severe phenotypical effect are easily obtained and studied by approaches of classical and molecular genetics. However, the nature of such mutations including those studied by Mendel [Mendel 1966] is mostly an inactivation of some gene or of its product [Bhattacharyya, 1990, Burrell, 1997]. It is highly questionable what role this type of mutation can play in evolution, for a discussion see [Bishop 1996]. On the other hand, most new traits that evidently played a role in the evolution of sexual organisms, i.e., increase or decrease of the size, changes of shape or proportions of organs are usually determined by many genes of a small effect. The evolution of biochemical or cellular functions probably occurred before the advent of multicellular organisms and in the absence of sexual processes. Therefore, these functions could evolve by standard neodarwinian mechanism. However, most of multicellular organisms‘ evolution should proceed by a different mechanism.
Finding conditions under which the heritability of phenotypic traits and heritability of fitness is sufficiently high can solve the paradox. Such conditions do not exist in outcrossing populations with the natural level of genetic variance. However, they do exist in populations with low level of genetic variance. Under natural conditions, such populations can originate due to colonization of a new geographic area or drastic reduction of population size (bottleneck effect) or by extremely assortative matting [Goodnight 1987; Whitlock et al. 1993]. In these populations, the genetic variance of the original population is drastically reduced by the founder effect and the subsequent effects of inbreeding. In asexual species with reduced genetic variance the effectiveness of natural selection and the rate of evolution is decreased as the selection has only limited reservoir of variants to select from. In sexual organisms the final effect of the variance decrease is very opposite, i.e., an increase of the rate of evolution. In the absence of genetic variance, the genomes of all individuals are same. Therefore, any new mutation occurs in offspring in the same (or very similar) genetic context as in the parent organism and the phenotypical effect of the mutation, as well as its effect on the fitness of any individual are the same. This means that the heritability of phenotypic traits and fitness of organism is high and the mechanism of neodarwinian evolution can operate generating evolutionary changes. Eventually, the natural level of genetic variance is renewed by mutation processes and the heritability of phenetic traits and of fitness decreases down to its original level.
It is well known, of course, that even the polymorphic populations can respond to selection pressure in an experiment. However, the response is known to be only transient and often reversible. Within a large, genetic-equilibrium population the frequence of various alleles is the result of dynamic competition of alleles with frequency-dependent selection coefficients (which can be predicted by an Evolutionarily Stable Strategies (ESS) approach). When we are putting a new selection pressure, we are in fact changing the pay-off matrix of the evolutionary game. The population must respond to such changes by shifting the equilibrium frequencies of particular alleles. After the end of the experiment (after several generations without the selection pressure and without any breeding program) the frequencies of alleles slowly return toward their original values. Of course, in small populations some alleles have been lost during the selection period, therefore the return cannot be perfect. In contrasts, the selection-induced changes in the large panmictic populations can be truly reversible.
It is important to stress that the same allopatric and sympatric isolation mechanisms that are considered to be a cause of cladogenetic processes of speciation are also responsible in sexual organisms for the functioning of anagenetic processes of origin of evolutionary novelties by means of natural selection. The proposed model shows that in sexual species the origin and development of new adaptive properties by means of natural selection are tightly associated with the origin of new species. Most of these anagenetic changes are probably concentrated only within the earliest period of the existence of a new species. After the accumulation of genetic variance the evolutionary plasticity of a species decreases or disappears. The species loses the ability to adaptively respond to changes of biotic and abiotic environment and for the rest of its sometimes long existence only passively waits for its terminal extinction.
The increase of rate of evolutionary (anagenetic) changes in the isolated populations has been observed in nature. The most divergent subspecies (including the largest and smallest ones) have been usually found on islands [Sondaar 1977; Angerbjorn 1986; Corbet 1986]. This contrasts with the predictions of Kimura‘s model of selection which suggests that the highest effectiveness of natural selection (higher probability of fixation of beneficial mutation) should be expected in subspecies with larger effective population [Kimura 1995; Kimura 1983]. This disagreement between the facts and theory is usually explained by postulating that most of the evolutionary changes in small populations were caused by fixation of slightly deleterious mutations by genetic drift [Ohta 1996]. Such mutations are effectively neutral in small populations but are selected against in larger populations. However, many changes observed in isolated populations, such as the increase or decrease of size, seem hardly selectively neutral and the rate of their fixation is unrealistically high for the genetic drift [Sondaar 1977]. Analysis of recently published results of experimental colonization of islands with Anolis lizards [Losos et al., 1997] shows that the rate of microevolutionary change correlates negatively with the founding population size. It is very important that the morphological changes observed in this experiment were of different intensity but in the same direction. Therefore, they can be promoted by relatively deterministic process of natural selection, rather than by stochastic process of genetic drift.
The largest amount of evidence for the model of vanishing heritability is accumulated in paleontological research. Paleontological data mostly support a punctualistic picture of evolution of multicellular organisms [Gould & Eldredge 1993] in which morphological changes of species are associated with the moments of speciation and for the rest of their existence an evolutionary stasis, i.e., the absence of anagenetic changes is characteristic. This contradicts gradualistic picture of evolution deduced from the neodarwinian model which supposed that most morphological changes should occur due to intraspecific selection operating during the whole existence of the species. According to this model most of adaptive changes should occur in large populations where the effectiveness of natural selection is the highest [Kimura 1983]. The cladogenesis and anagenesis should be two independent processes. In contrast the vanishing heritability model suggests that the capacity to evolve a new adaptive trait in a large stabilized population with a natural level of variance is highly limited, if any. Most of adaptive changes in sexual species can evolve in small genetically isolated populations under conditions of decreased variance and increased heritability of fitness, i.e., in the earliest period of the existence of a new species.
Finally, the model also explains the association between major evolutionary changes and mass extinctions [Raup 1994]. In the period of mass extinction, the population size of many species is drastically reduced. This results in the decrease of population variance and following increase of heritability of fitness. After the mass extinction the size of populations returns quickly while the variance slowly toward its original value. Consequently, evolutionary plasticity and potential of the species that passed through the bottleneck of mass extinction is transiently renewed. The phenomenon of the evolutionary burst after the mass extinction is again in contradiction with implications of Neodarwinian model of evolution by means of (intraspecies) natural selection. After the end of mass extinction the population sizes of most species probably grow. In this period the intensity of intrespecific competition and consequently of the selection and evolution would decrease rather than increase.
The present hypothesis represents an alternative model for evolution of adaptive traits in sexual species. It suggests a solution for various biological problems that until now resisted explanation within a framework of neodarwinian theories. A corner stone of the hypothesis is a model of vanishing heritability of phenetic traits and biological fitness in outcrossing populations. From the time of the victory of Modern synthesis in evolutionary biology, the „hard“ heritability of phenetic traits has rarely been doubted and virtually never seriously tested. The current methods of estimation of heritability of phenetic traits measure the correlation between expression of the trait in close relatives, i.e., the expression of the trait in the context of very similar genomes. Therefore, these methods cannot reveal the vanishing nature of biological heritability. The experiments studying the rate of evolutionary change in small and large or inbred and outbred populations do not distinguish between the short term effect of fixation already present genetic variance and the long term effect of higher heritability of fitness and better chance of fixation of new mutations. All these technical problems, however, can be easily avoided and the question of existence and prevalence of vanishing heritability of phenetic traits and biological fitness can be experimentally resolved.
A corner stone of the hypothesis is a model of vanishing heritability of phenetic traits and biological fitness in outcrossing populations. From the time of the victory of Modern synthesis in evolutionary biology, the „hard“ heritability of phenetic traits has rarely been doubted and virtually never seriously tested. The current methods of estimation of heritability of phenetic traits measure the correlation between expression of the trait in close relatives, i.e., the expression of the trait in the context of very similar genomes. Therefore, these methods cannot reveal the vanishing nature of biological heritability. The experiments studying the rate of evolutionary change in small and large or inbred and outbred populations do not distinguish between the short term effect of fixation already present genetic variance and the long term effect of higher heritability of fitness and better chance of fixation of new mutations [Katz & Young 1975; Bryant, et al. 1986; Bryant, McCommas, & Combs 1986 Lopez-Fanjul & Villaverde 1989]. All these technical problems, however, can be easily avoided and the question of existence and prevalence of vanishing heritability of phenetic traits and biological fitness can be experimentally resolved.
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