Microevolutionary, macroevolutionary, ecological and taxonomical implications of punctuational theories of adaptive evolution

Microevolutionary elasticity and adaptation to past condition

According to the classical gradualistic theories, all species respond to selection as if they were plasticine while, according to punctuational theories, most species are resistant to selection as if they were lead (class II and class III theories) or respond to selection as though they were rubber – at first, they respond readily to selection pressure; however, as the average phenotype of the organism deviates from its original state, selection is less and less effective and, at a certain point, the response ceases (class IV or class V theories) (Table 2). According to class IV and class V punctuational theories, the average phenotype returns to the original state when the selection stops [3].

There are several critical implications: in the world of species that do not respond to selection, organisms are not optimally adapted to the conditions of their current environment but to those present during the evolutionary plasticity of the particular species. This should be true especially for evolutionarily old species, as their environmental conditions probably differ most from those existing during their origination. For example, algae (the typical representatives of ultrabradytelic species), which originated in the Paleozoic when days lasted about 21 hours, are known to better synchronize their circadian rhythms with shorter light–dark cycles than the current 24-hour cycle [4].

Lower Viability and Fertility of Selected Organisms

Representatives of old, either microevolutionary frozen and therefore “obsolete” species (class II and III theories) or elastic species, kept out of their original state by selection (class IV and V theories), have lowered viability or fertility in comparison with representatives of young species living under conditions similar to those existing at the time of their origination [3]. Therefore, the population density is probably negatively correlated with species age; a study of the correlation of the molecular age of a species with its average abundance could easily test this prediction.

The correlation could also explain the existence of the most universal ecological law – that every community shows a hollow curve on a histogram with many rare, and only a few common species [5]. This is a quite stable situation; species retain their basic status as common or rare for millions of years [6]. Class II-V punctuational theories of evolution predict that common species are young species, still evolutionarily plastic or having recently lost their plasticity, that still live under conditions similar to those existing at the time of their origination. This agrees with the observed correlation between global and local abundance in young species, but not in old. Old species are probably less competitive in a similarly broad spectrum of biotopes as young species [7]. Class II-V punctuational theories of evolution also predict that the paleontological record will more often show a gradual change from common to rare species rather than the opposite change from rare to common species.

Limited Geographical Range of Species

On the basis of class IV and class V theories, it can also be expected that populations near the center of the species’ range express higher mean viability or fertility than those on its periphery, which have had to adapt to conditions different from those at the time of its origination. E.g. tits are able to adapt to a different climate, with its corresponding shift in peak abundance of caterpillars, by a shift of their own breeding season. However, the fertility of these adapted populations decreases in comparison with birds adapted to the original climate [8, 9].

Negative correlation between deviation from the equilibrium frequency of alleles (and from the original phenotype of the species) and the fitness predicted by any class IV and class V punctuational theory of evolution could provide an alternative explanation for the existence of distinct geographic ranges of species. Elastic species can adapt to geographically changing conditions only to a certain degree. At some point, the decrease in fitness accompanying the departure of the phenotype from the original state is so great that it is incompatible with the long-term survival of the population.

Lower Viability and Fertility of Decorative Breeds

The same negative correlation between departure of a phenotype from the original state and the mean fitness could explain the lower viability and fertility of most decorative breeds of practically any domesticated species. When the populations of pure-bred animals are left to their fate, members of the population return to the phenotype of their wild predecessors within a few generations. This phenomenon differs from the return of the phenotype to an original wild form in the case of crosses between two different races. In crosses, the almost immediate return to the original phenotype is caused by a breakdown of the unique combination of alleles (responsible for the appearance of the members of the individual races) as a consequence of recombination and segregation of alleles. In members of the same race, there is a gradual return to the wild phenotype as a consequence of the action of natural selection which, during a few subsequent generations, removes from the population the individuals with reduced viability and fertility, i.e. with the phenotype of the human-bred race.

Coexistence of Species that Use the Same Resource

The absence of evolutionary plasticity predicted by class II, III, IV and V punctuational theories could also explain long-term coexistence of species that use the same resource. Theoretical analysis shows this coexistence is possible, but highly unstable in evolutionarily plastic species [10]. Sooner or later, one of them increases in exploitation intensity or efficiency, thereby causing the extinction of the competing species. The absence of evolutionary plasticity in sexual species could be an important positive factor in the conservation of global and local biodiversity.

Efficiency of Group Selection in Non-plastic Species

The low and vanishing inheritance of phenotypic traits in polymorphic sexual species predicted by class III, IV and V punctuational theories could also explain the persistence of altruistic behavior and general efficiency of group selection. The most serious objection of evolutionary biologists against the role of group selection in evolutionary processes consists in the fact that a trait that provides an advantage to a group and simultaneously places the individual that is its carrier at a disadvantage has a low chance of spreading and enduring in nature. Groups in which the altruistic trait spreads would prosper better than groups in which this trait is lacking and the average fitness of the members of this group would be greater; however, selfish individuals who do not exhibit this trait and do not behave altruistically, but only enjoy the advantages provided by the presence of altruists, would have the greatest fitness within these groups. In sexual (elastic) species, any behavioral trait (for example, altruistic behavior) is usually determined by the greater number of genes and many of these genes have (due to epistasis) a context-dependent influence on the particular trait. Consequently the heritability of most traits is low. Under these conditions, altruists emerge from the population as if by chance in families that are completely unrelated and have different phenotypes, i.e. individuals with quite different behavior, with a probability that is determined only by the proportion of particular alleles in the entire population. Thus populations can compete for the greatest average fitness of their members; those that have the greatest proportion of the relevant alleles, resulting in the greatest number of altruists being formed (emerging by chance), will win in this competition. The models show that group and inter-species selection can occur in nature in favor of altruistic traits (because the percentage proportion of alleles in the population is inherited from one generation to the next) and its results cannot be cancelled out by individual selection because the trait itself, altruistic behavior, is not inherited [11].

Existence and Success of Invasive Species

The existence of two species types, very common non-plastic (microevolutionary frozen, according to class II and III theories or elastic, according to class IV and V theories) and very rare plastic, offers a new explanation for the existence of invasive species. The transfer of a species to a new territory is a necessary, but not sufficient, condition for invasion. In the vast majority of cases, the species succumbs to competition with local species and dies out. Only a small fraction of introductions “succeed”. For example, red deer were introduced into New Zealand a total of 32 times and only the last attempt was successful; however, these deer now occupy the entire area of the southern island [12]. Similarly, the now excessively successful starling settled in America only after at least nine attempts [13]. Invasive success is usually preceded by a relatively long lag phase, in which the future invasive species peacefully coexists with native species in the limited area of their original introduction.

According to classical gradualistic evolutionary theories, native species, which are adapted to local conditions, should outcompete newly introduced species [14, 15]. According to the discussed class II-V punctuational theories, the ecological success of some newcomers is not very surprising. During the introduction and lag phase, the genetic polymorphism of an introduced population decreases, which could result in the conversion of a non-plastic species to the plastic state [16]. Non-plastic 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 non-plastic species in the coevolutionary arms-race.

Data on the evolutionary plasticity (evolvability) of invasive species are rather scarce [17–19]; however, e.g., the invasive grass Phalaris arundinacea demonstrates greater heritability and higher evolutionary plasticity (greater response of the phenotype to the local conditions) in North America than in its original area in Europe [20]. In accordance with the predictions of punctuational theories, parthenogenetic species (which always have much greater heritability of fitness than sexual species) [21] and polyploid species (which have often slipped through a genetic bottleneck as species of peripatric origin) [19] are over-represented among invasive species.

Low Efficiency of Domestication of Plant and Animal Species

The existence of only a low proportion of evolutionarily plastic species can also explain the fact that humans have succeeded in domesticating only a negligible number of plant and animal species [22]. Only plastic species can adapt to the drastically changed conditions of life in captivity without a substantial reduction in viability and fertility. Class III, IV and V punctuational theories of evolution explicitly or implicitly suggest that domestication should be successful mostly in young, unfrozen species. It is worth recalling that most selection experiments were performed either on domestic animals, probably with lower genetic variance from the very beginning, [22] or on small populations that had passed through a narrow bottleneck just before, or at the beginning of, the experiment. Therefore, the ability of a species to respond to selection is probably overestimated and the natural elasticity is underestimated by the results of these experiments or of long-term selection programs performed on domesticates [23].

Class III, IV and V punctuational theories predict that most varieties of domesticated plants would have been derived from species with a capacity for vegetative reproduction, e.g. by means of tubers, rhizomes or grafts, or from self-pollinating species [22]. The plasticity of asexual species is higher than that of sexual species, and that plasticity is greater in self-pollinating species than in cross-pollinating species [24]. Therefore, these species can be more readily changed by artificial selection. On the other hand, sexually reproducing and cross-pollinating varieties should be more stable and lose properties acquired by artificial selection more slowly. Due to natural selection, a plastic variety has a tendency to increase its fertility at the expense of properties useful for man. In contrast, a sexually reproducing (elastic) variety can only respond to selection to a certain degree, and therefore cannot lose its useful properties due to natural selection. It was reported in the older literature that the varieties of cross-pollinating rye usually remained in seed company catalogues much longer than did those of self-pollinating wheat [24].

Success of Asexual Species in Habitats with Extreme Conditions

The plasticity of asexual species should be greater in habitats that are poor in resources or where survival is limited 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 environmental requirements. It is noteworthy that asexual species or asexual lineages of otherwise sexual species are found primarily in habitats with extreme conditions – in habitats that are extremely dry, cold or poisonous. The proportion of asexual species increases, for example, with increasing altitude and latitude, or where the soil contains high concentrations of poisonous heavy metals [25, 26]. On the other hand, elastic sexual 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 arm-race plays the crucial role. The fact that they retain most of their genetic polymorphism enables them to rapidly respond to any selection pressures by shifting the frequencies of their alleles without needing to wait for rare advantageous mutations.

Evolutionary passivity of elastic species and the advantage of sex

Elasticity of sexual species predicted by class IV and V theories or evolutionary passivity of sexual species predicted by class III theories could also be advantageous in a long-term perspective. Under the fluctuating conditions of a stochastic environment, plastic asexual species could adapt to transient environmental change while non-plastic species resist such a change of their phenotypes. When the environmental conditions return to normal, a plastic species could fail to return to its optimal phenotype rapidly enough to avoid the risk of extinction, while the population of an elastic species (class IV and V theories) returns to its original phenotype within a few generations and a population of microevolutionary frozen species (class III theories) stays near the original optimum all the time. As suggested by G.C. Williams [27], the main advantage provided by sexual reproduction could consist in a substantial reduction in the evolutionary capability of sexual species. As a consequence of their elasticity and/or frozenness, sexual species are evolutionarily passive throughout much of their existence and cannot opportunistically respond to temporary short-term changes in the external conditions.

Coincidence of Changes of the Phenotype of Organisms with Speciation

According to gradualistic models, there should be no correlation between cladogenesis and anagenesis (between speciation and changes in the phenotype of organisms) while punctuational models of any class assume that major irreversible phenotypic changes are always associated with speciation. The opposite does not hold, as most speciation events, such as vicariant allopatric speciation, parapatric speciation and many forms of sympatric speciation, are not coupled with a dramatic reduction in genetic polymorphism and return to plasticity. These forms of speciation could be responsible for the origin of most species, while new genera or higher taxa (i.e. monophyletic lineages with characteristic prominent evolutionary novelties) mostly result from peripatric speciation. Therefore, punctuational theories of evolution predict that the number of evolutionary changes in phenotype in a phylogenetic lineage reflects the number of speciations in this line rather than its age. A study of passerine birds has found the number of speciation within a phylogenetic line to have a very strong effect on the rate of anagenesis. The number of species alone explained 33.3% of the total variation in morphology [28]. Moreover, the reported rate of anagenesis on islands seems to be higher than on the mainland [28]. The higher frequency of peripatric speciation on islands can be a clue for explanation of the observed phenomenon.

Another corollary of the anagenesis-cladogenesis association predicted by the punctualistic models of evolution is that the extant representatives of ancient phylogenetic tree branches that have sustained a lower number of speciation events should bear more plesiomorphic characters than representatives of apical branches of the phylogenetic tree. According to classical gradualistic theories of evolution, no such correlation between species age and its antiquity should be expected.

Correlation between the Rate of Molecular Evolution and the Speciation Rate

The correlation between the rates of anagenesis and speciation can be detected even on a molecular level. A molecular study [29] 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. Of course, a large part of the monitored nucleotide substitutions are neutral mutations known to be fixed by means of genetic drift and genetic draft and not by selection. Drift probably operates at the same rate in frozen, elastic and plastic species, however, the genetic draft operates more effectively during plastic phase of evolution when many neutral and nearly neutral mutations are being fixed with positive mutations by genetic hitchhiking. Approximately 35% of the substitutions (20-70%, depending on the studied taxon) was shown to occur in brief periods of speciation. It is worth mentioning that we are not aware of how many speciation events actually occur in the studied, seemingly unbranched lineages. Therefore, the published estimates of speciation-associated substitution rates represent only the lower margin of the real figures.

Molecular studies also confirm increased rates of evolution in island species. These species have not only a higher substitution rate but also a higher frequency of nonsynonymous substitution among the observed mutations, which suggests that positive selection rather than drift plays a more important role on islands (where a higher frequency of peripatric speciation is expected) [30]. Of course, another explanation for observed higher nonsynonymous substitution rate in island species, namely the higher probability of fixation of slightly negative mutations during peripatric speciation, also exists.

Punctuational Evolution and the Origin of Evolutionary Trends

The class II-V punctuational models of evolution also offer a new explanation for the existence of evolutionary trends, the slow directional phenotypic changes in organisms of particular phylogenetic lineages that endure much longer than the individual species involved. The trends are too slow to be geared by selection – the change in the value of the trait per generation is so small that it is completely invisible for selection [31], p. 835. According to gradualistic evolutionary theories, the selection pressure has to be sufficiently strong to overcome genetic drift. However, this type of selection should result in far more rapid changes than those that emerge as trends in the paleontological record. Punctuational theories suggest a new solution to the paradox of very slow evolutionary trends. According to punctuational theories, 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 the brief and rare periods of their evolutionary plasticity.

Shrub-Shaped rather than Tree-Shaped Phylogenetic Trees

Long-term, the number of species on Earth is relatively stable or even increases [32–35]. Thus, if some species become extinct without speciation, then other species must necessarily undergo speciation a great many times. It is therefore highly probable that a species in a transiently plastic state splits off not one but several different species. It has already been pointed out that the shape of phylogenetic trees differs significantly from that predicted by the neutral model of random speciation and extinction [31, 36]. Phylogenetic trees are usually shrub-shaped rather than tree-shaped. Most disparate species originate simultaneously from a common ancestor as a result of adaptive radiation. Particular species that 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 that could undergo a new burst of radiation. Interestingly, such a tree is similar in shape to the figure drawn by Darwin [37] and unlike modern trees (which are usually automatically interpreted as phylogenetic trees but are in fact inspired by the shape of the cladogram, a graphic representation of the distribution of synapomorphies within a taxon).

Higher Variability of Early-Branched Species and Decreasing Speciation Rate of Clades

The decreased variability of species with age of the phylogenetic line and the maximum biodiversity achieved early after the origin of the phylogenetic line [38, 39] are other phenomena that are not supported in gradualistic evolutionary theories but are explicable within class V punctuational theories. Webster [40] reported that the frequency and extent of morphological variations in 982 trilobite species are greatest early in the evolution of the group. He has shown that “the proportion of species with at least one polymorphism drops sharply between the Middle Cambrian (75%) and Late Cambrian (8%), then rises to 40% in the Early Ordovician (coincident with the first sampling of the diverse phacopid and proetid orders), after which there is a progressive decline through the Middle Devonian (1%), interrupted only by a particularly low value (0%) in the Late Silurian. No polymorphism was recorded in character-state coding among the 23 post-Devonian species [41]”.

Change in the diversity of a clade (but not necessarily the abundance of a species) is usually asymmetrical in time; a clade quickly achieves maximum diversity and slowly goes extinct [39, 42]. In addition, the speciation rate usually declines with increasing age of a clade [43, 44]. Both phenomena could have a common cause, continuous irreversible freezing of more and more traits during the evolution of a clade [3]. Traits differ in resistance to transition from frozen to plastic in response to reduction of genetic polymorphism. For some traits, this is likely to happen readily, coupled with a relatively small reduction in genetic polymorphism. For others, transition from frozen to plastic is difficult or even impossible, as it requires an unrealistically long period of persistence of an unrealistically small population. On a macroevolutionary time-scale, more and more traits that are characteristic for the clade (or rather the corresponding taxon) pass into the permanently frozen state due to a universal process of sorting for stability. Stable traits (systems etc.) persist while unstable traits (systems, etc.) pass away. A stable trait is a trait coded by many genes that are interchangeable in their effect. The mutation of an allele in one locus does not result in a change in such a trait, while mutation in all the loci is highly improbable especially if, due to pleiotropy, the genes in particular loci also influence other traits. Another source of the evolutionary stability of a trait is frequency-dependent selection, particularly the steep dependence of fitness on the frequency of an allele. When the fitness of an individual decreases sharply with the increased frequency of an allele (of a particular trait), even a drastic reduction in population size cannot lead to total loss of the polymorphism in a particular locus. Due to dominance, and especially to epistatic interactions of more than two genes, the slope of fitness can be very steep. In the dominance case, the fitness of homozygotes with genotype aa could decrease at a rate proportional to the second power of the trait frequency. In the case of epistatic interactions between more than two genes, the rate could be proportionally higher. This kind of trait probably survives peripatric speciation in a polymorphic state, or polymorphism in such a trait is restored very quickly in the newly emerging species due to mutations.

In a new taxon, i.e., a clade that was named by taxonomists because of the presence of certain combination of (‘important’) traits, a relatively high proportion of species contain many apomorphic traits that could become unfrozen during standard peripatric speciation or that are relatively plastic even at the level of a species (or even of a local population). In time, more and more traits in more and more species turn to a semi-permanently or even permanently frozen state. The representatives of a particular taxon 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 future peripatric speciations. Originally, many representatives of a taxon had the capacity to evolve new body plans after peripatric speciation. In the end, only some species retained this capacity and, even in these species, some traits had a highly limited capacity to respond to selection after peripatric speciation.

Dead Clade Walking

This last mechanism can explain another well-known phenomenon, namely: dead clade walking. It is widely known that unexpectedly many diversified and diversifying clades that survive a period of mass extinction turn marginal or decline in the aftermath stage. Jablonski [45] wrote that “For four of the Big Five mass extinctions of the Phanerozoic, the marine genera that survived the extinction suffered about 10–20% attrition in the immediately following geologic stage, significantly greater than the losses sustained in pre-extinction stages. The stages immediately following the three Palaeozoic mass extinctions also account for 17% of all order-level losses in marine invertebrates over that interval, which is, again, significantly greater than for other stratigraphic stages (no orders are lost immediately after the end-Triassic or end-Cretaceous mass extinctions).” Such a pattern could be expected when all the representatives of a clade that survived the mass extinction were irreversibly frozen [3]. A clade depleted of all the species that can be turned plastic by peripatric speciation cannot adapt to the changing environment and would probably become extinct in the next chronostratigraphic stage.

Cambrian Explosion

Another phenomenon that cannot be explained within the traditional gradualistic evolutionary theories is the Cambrian explosion [46, 47]. All the basic animal architectures were apparently established by the close of the Cambrian explosion; subsequent evolutionary changes, even those that allowed animals to move out of the sea onto the 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 10–20 million years during the Cambrian , and remained stable or even decreased throughout the following 500 million years [46, 48]. The number of species increased irregularly and discontinuously during the Phanerozoic; however, the number of body plans, i.e. disparity, probably decreased.

Considerable efforts have been exerted to suggest that the Cambrian explosion, a phenomenon that had no support in contemporaneous gradualistic evolutionary theories [49, 50], is not in any way mysterious or that it never even occurred [51–54]. Molecular clock data based on concatenated amino acid sequences of 129 proteins from 36 eukaryotes suggest that representatives of metazoan phyla probably diverged 100–210 million years before the Cambrium [55]. (Previous molecular studies suggested an even earlier divergence time; however, the results of current multigene studies are more reliable.) Nevertheless, this molecular data is useful for tracking events of cladogenesis, but not events of anagenesis [56]. The metazoan phyla could diverge long before the Cambrian; most probably, however, their representatives had very uniform body plans until the beginning of the Cambrian when some extrinsic (ecological) or intrinsic (genetic) event probably triggered the morphological diversification of the Metazoa.

The Cambrian explosion is in accordance with predictions of class V punctuational theories. At the beginning of the evolution of the metazoan clade, many traits, even those that determine body architecture, had the capacity to turn plastic during peripatric speciations in many metazoan lineages. Therefore, both radical remodeling of body architecture as well as novel origination therein were possible in the early stages of metazoan evolution. Through time, more and more traits became 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 came to be based on modification of existent plans rather than creation of new ones. Were something, e.g. a virus or humankind, to kill all the metazoan species on Earth with the exception of a single cockroach species, classical evolutionary theories argue this species would differentiate into many new phyla with radically different body plans to exploit all the available niches. The frozen plasticity theory explicitly argues [3] that it would differentiate into many new species of cockroaches, leaving most niches empty.

Objective Existence of Species and Genus Taxonomic Categories

The punctuational theories suggest that the taxonomic category of species, and sometimes even that of genera and higher taxa, could objectively denote the existing entity, rather than merely being a useful epistemological construct of biologists. Within any punctuational theory, a biological species can be defined as a set of individuals sharing an identical gene pool throughout the period between two speciation events. Similarly, within class III-V punctuational theories, a genus can be defined as a set of individuals sharing a common exclusive ancestor in the period between two periods of evolutionary plasticity.

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