Shishkin (2015) Evolution as the Maintenance of Organizational Stability

Shishkin M.A. Evolution as the maintenance of organizational stability // Morphogenesis in individual and historical development: stability and variability. - Moscow, 2015. Pp. 70-75. EVOLUTION AS THE MAINTENANCE OF ORGANIZATIONAL STABILITY M.A. Shishkin Paleontological Institute named after A.A. Borissiak, Russian Academy of Sciences shishkin_paleo.ru I The transition of a physical system from one state to another (a phase transition) occurs through the growth of its instability near the point of transformation, when fluctuations of the existing internal connections within the system reach a critical amplitude, and their rupture ultimately ensues. The evolution of organisms as dissipative dynamic systems existing in a state of "flow equilibrium" obeys the same regularity (cf. Volkenstein, 1984). The transformation of such a system toward a new stable terminal state, which is in equilibrium with the environment and is termed the adaptive norm, constitutes a phase transition. It implies that, under the given altered conditions, the previous state of the system has exhausted its regulatory capacity, i.e., its capacity for self-maintenance. Thus, in the course of the evolutionary process, two principal categories of states alternate regularly: stable states and relatively unstable (more transient) ones. They are registered as changes in the character of variability of living organization at a chosen scale of assessment, ranging from the state of populations to higher levels of consideration. The phenomenon of elevated initial variability during the establishment of a new structural plan has been empirically recognized by investigators since Charles Darwin, who regarded individual variations as the starting point of changes leading to the formation of a species. Manifestations of this feature are also common in the paleontological record (e.g., Simpson, 1948; Van Valen, 1969). The purposive behavior of organisms, for whose explanation the idea of evolution serves, is an expression of their stability. In relation to species organization, this property expresses the stability of its self-maintenance (adaptability) and ontogenetic self-reproduction (heredity). Explaining the evolutionary process is answering the question of how, when conditions change, the disrupted stability of a living system can subsequently be restored at the cost of a reorganization of the system, bringing it to a new equilibrium with the environment. Solving this problem on reductionist grounds is impossible, since for the linear determinism accepted in that case there is in general no problem of stability as a subject requiring explanation. Stability is understood here as an a priori property of the elements that determine development. But from the experience of embryology - both comparative (Baer's second law) and experimental (generalizations of Driesch, Gurwitsch, and others) - it is known that the whole in development is not a derivative of its parts, and, conversely, itself determines their state, beginning with the zygote. Therefore, an explanation of evolution is possible only on the basis of an organismocentrist theory. It must not only acknowledge the existence of internal regularities in the evolutionary process (as does Lamarck's gradualism or the idea of nomogenesis), but also explain their essence. These conditions are best met by the epigenetic theory of evolution (ETE), which regards the organism as a stable developmental system in which all responses are determined solely by its own specificity, independently of the nature of the perturbations (Goldschmidt, 1940), and which is transformed by natural selection as a whole (Schmalhausen, 1982; Waddington, 1957). From this standpoint, the directionality of development toward the norm is understood as the result of its systemic regulation toward a canalized trajectory of changes. Deviations from the latter, potentially leading to phenotypic aberrations, manifest themselves in the great majority of cases merely as fluctuations that are relaxed during the course of ontogenesis. But as developmental conditions shift beyond the limits permitting regulation, the capacity to dampen fluctuations decreases, leading to a critical increase in the frequency of disruptions of the adult norm. The uniform developmental outcome for individuals is replaced by a spectrum of labile aberrations (morphoses) specific to the given system and inherited in an unordered manner across generations (the so-called "release of cryptic variability"). The competition among these alternatives under the newly prevailing conditions signals the engagement of natural selection. This moment of systemic instability is the beginning of the potential transition to a new organizational plan. Thereafter, selection in favor of the preserved morphosis leads to an increase in the reliability of its individual reproduction across generations (among genetically non-identical individuals). In this way it acquires the status of a new norm. The increase in its stability is a consequence of the reorganization of the formative mechanisms of development, which begins with the terminal stage directly preserved by selection and deepens over successive generations. The key characteristics of the transformed state of the system are the establishment within it of a new canalized trajectory and the reorganization of the former space of deviant trajectories, together with a change in the probability of their realization under one or another set of particular conditions. In the conceptual framework of ETE, the above account represents the picture of an elementary evolutionary event, comprising the destabilization of the previous norm and a step toward the creation of a new one on the basis of one of the variants of the "perturbed" state of the former. Selection is understood here as a mechanism of self-organization, i.e., the search by a disrupted system for a new equilibrium through the fixation of one of the developmental deviations. An evolutionary change is evidence that under the new conditions the possibilities for individual regulation are exhausted, and their restoration requires a reorganization of the system itself. The sequence of unidirectional elementary steps of this kind leads to the historical accumulation of changes determined by the initial choice. From this understanding of evolution as a systemic transformation, a number of expected consequences follow. (1) The characteristics of systems in related forms should be similar, displaying analogous sets of ontogenetic trajectories realizable for them (with varying probabilities). This should be expressed in close similarity of variability spectra, especially for the principal, most discrete variants. (2) Elements of the spectrum realized in some taxa as variations will have the status of norms in others. (3) A labile aberration induced by a disruption of developmental conditions can be fixed by selection, i.e., become stably reproducible across generations. (4) The morphogenesis of an evolutionary novelty that arose in the conditions of adult life and was originally dependent on those conditions will, in the course of evolution, change in the direction of (a) autonomization from that dependence, (b) ever-greater integration with other formative processes, and (c) the displacement of its initial manifestation to earlier stages. (5) Any structure (or organizational plan as a whole) is always historically older than the mode of its realization in a given type of ontogenesis. All these regularities are known in reality. Phenomenon (1) is reflected in a multitude of generalizations indicating the orderedness of structural variation manifestation (including the distribution of anomalies). These include Darwin's "analogous variation," Vavilov's "homologous series of variability," Krenke's "law of related deviations," as well as overlapping or synonymous concepts introduced by S.V. Meyen ("refrains," "transitive polymorphism," "polymorphic sets"). More generally, the limitation of morphogenetic pathways for each type of zygote is implied by the concept of the "norm of reaction" (in the sense of W. Johannsen; cf. Kamshilov, 1967); this same regularity underlies the nomothetic conceptions of L.S. Berg. Today it is widely employed under the designation "developmental constraints" in attempts to modernize the neo-Darwinian understanding of evolution. However, no genuine alternative to the systemic explanation of R. Goldschmidt - adopted by ETE (see above) - has yet emerged in its interpretation. One of the explanations proposed (Berg and his followers) is to attribute the orderedness of the space of variations to supra-biological laws of the material world. The notion of the independence of this property from natural selection is in general characteristic of views not connected with ETE. The consequence (2) noted above is likewise confirmed among the enumerated generalizations. It is illustrated by countless examples where a stable character of a taxon has parallels in the form of variations of any nature or particular modifications in other related forms. For these analogies, as in the first case, there is no convincing explanation other than the idea of holistic responsiveness of the developmental system (grown out of Goldschmidt's experiments on phenocopying mutational effects). Moreover, the qualitative distinction, common in genetic thinking, between "hereditary" (stable) and "non-hereditary" (condition-dependent) responses altogether precludes any explanation of their similarities other than chance. Consequences (3-5) attract far less attention from investigators. The reason for this is evidently their difficult compatibility with the habitual conviction that evolution proceeds, like ontogenesis, through changes from the germ cell to the adult state (in fact the opposite is the case, see Shishkin, 2010, 2012, 2014). These consequences, especially (4, 5), demonstrate that equifinality in the realization of adult organization (i.e., the starting point of evolutionary transformations) takes place not only in species-specific ontogenesis, but manifests itself in one way or another on the scale of the entire history of a given structural plan. Among the above propositions, conclusion (3) - the increase in the heritability of labile characters when they are preserved by selection - is demonstrated by experiments on the stabilization of induced morphoses (Waddington, 1957). Consequence (4) is confirmed by comparative data showing that the morphogenesis of a character that arose in adult-life conditions and is sensitive to their parameters becomes historically increasingly freed from such dependence (including conditioning by adult function) and from a predominant association with the end of development (Schmalhausen, 1982; Shishkin, 1988, 2010, 2012). An instructive illustration of consequence (5) is provided by examples in which the same organizational plan in related forms, or simply within a single species, can arise on the basis of different and sometimes clearly sequential developmental pathways - including differences in sex determination, mode of reproduction, character of transformation (direct or with metamorphosis), and so on. Taken together, these features (1-5) demonstrate the predictable holistic characteristics of the developmental system and their regular dynamics in the course of the stabilization of novelties. II As already noted, the structural orderedness of organisms, built by selection each time on the basis of a more labile and inharmonious state, has different scales of manifestation, not restricted to the level of steps leading to the replacement of species norms. At the level of taxa uniting species and larger communities, the two basic organizational states under discussion have different characteristics from those at elementary evolutionary events, and alternate far less frequently than in that case. The stability of an established group is expressed in the presence among its members of a syndrome of basic features marking the belonging of these forms to a common segment of conservative "gradual" evolution - within the framework of the structural plan formed beforehand. For the phase transition occurring upon the collapse of this plan and its further transformation into a different model, the overall variability of states is described no longer in terms of individual variability, but as a disorder in the diversification of taxa arising in the course of such a transition. This last feature, or "archaic diversity" (Mamkaev, 1968, 1991), is expressed in the presence within the new group of a series of basal forms or lineages with grotesque combinations of individual features corresponding to the distinctions of existing or future groups of high rank. Observed at a specific temporal cross-section, such a picture represents preserved traces of attempts by an ancestral organizational plan, having lost stability, to find (through reorganization) a new equilibrium in altered conditions - on the basis of its non-equilibrium variants. Being directed toward the acquisition of such a state, these attempts, regardless of the degree of their success, inevitably turn out to be variations on a single theme (the search for an optimal structural plan), with the majority disappearing relatively early. Since, as already stated, the loss of stability of the original species norm means the appearance in its place of a multitude of non-equilibrium deviations, and since these constitute the only substrate for the search for a new equilibrium, it should be supposed that the history of a new structural plan must always begin with the appearance of a spectrum of alternative, weakly stable, unidirectional basal lineages. That is, the variant that ultimately prevailed (and was further transformed) was at first merely one of many. In other words, "archaic diversity" is a regular initial stage of phyletic evolution, regardless of the degree of its paleontological documentation in each particular case. Manifestations of initial organizational disorder, being in most instances relatively transient and local, are on the whole poorly captured by the geological record. But their most notable traces, reflecting structural changes of varying scale, may be fragmentarily preserved with one degree of completeness or another. Therefore, the principle of initial instability of evolutionary novelties has been reflected directly or indirectly in many generalizations based on paleontological material. These are: the absence of transitional forms from the fossil record (noted already by Darwin), the concept of "punctuated equilibrium" in species evolution, and in particular the conceptions of "quantum evolution" (Simpson, 1948) or "incoherent evolution" (Krasilov, 1986). The principal features of this disordered evolutionary phase, noted in the above generalizations (see Simpson, 1948; Simpson, 1953; Grant, 1980; Rasnitsyn, 2002), have been largely discussed above. These are: (1) the accelerated pace of change; (2) the non-equilibrium character (reduced adaptability) of transitional states on the path to a new organizational plan; (3) the high level of their variability, and, if this is assessed at the level of taxon diversification, the manifestation among them of the phenomenon of "archaic diversity"; as well as (4) the confinement of the beginning of these events to small isolated populations. It is recognized that the primary stimulus for such transformations must be major environmental changes in time or in space, under which the survival opportunities of organisms in intermediate conditions are extremely limited. In the former case of such changes, the most large-scale events are represented by biotic crises; in the latter, by one or another abrupt shift of adaptive zones (for example, during colonial or island dispersal). The connection between the indicated shift of conditions and the unusual features of structural diversification on the path to a new structural plan appears obvious. The disruption of morphogenetic regulation ensuing from such a shift leads to the replacement of the stable species norm by labile non-adaptive aberrations, whose selective survival depends on the speediest possible stabilization within the framework of some variant of the new conditions. On the other hand, the liberation of the species from the strict control of the former biota immediately broadens the space of possible stabilization pathways for derivatives of the former norm. Together these two factors potentially provide for the origin, in place of the latter, of a multitude of temporary particular adaptations formed extremely rapidly - through simple one-sided changes ensuring equilibrium (viability) only within extremely narrow ranges of conditions. Their subsequent selective evolution in the same directions constitutes the basis of "archaic diversity." This imbalance of transformations is an example of what is called inadaptive evolution (Simpson, 1953; Rasnitsyn, 2002). It also renders apt the comparison with artificial selection (Krasilov, 1986). But the similarity with the latter consists not in "reduced competitiveness," as has been suggested (in the stabilized morphotype it is, on the contrary, higher than in the initial morphosis), but precisely in the one-sided character of the fixed changes. These generalizations allow us to understand the meaning of the phenomenon of "senile variability," i.e., the unusual structural diversification of phyla sometimes noted in the terminal stages of their existence. We see here direct confirmation of Simpson's conjecture (Simpson, 1948; Simpson, 1953) that in this case the subject is the initial search for a transition to a different organizational plan, i.e., the non-equilibrium phase of the evolutionary event under discussion, termed by this author a "quantum shift" - regardless of whether this transition was actually accomplished. One need only add that the multiplicity of terminal branches of such a declining phylum, demonstrating, in Simpson's view, its exploratory behavior in alien conditions under the action of "centrifugal selection" (in reality the stabilization of alternative deviations), constitutes, as emphasized above, a general regular manifestation of the disorder of the initial stage on the path to organizational transformation. It is precisely this disorder that generates "archaic diversity." The foregoing considerations are confirmed by the analysis of traces of structural disorder observed during the transition from the Paleozoic organizational plan to the Mesozoic ("stereospondyl") plan in dominant ancient amphibians (Temnospondyli) across various phyletic lineages throughout the Permian-Triassic ecosystemic crisis (Shishkin, 2013; Shishkin, 2014). It is shown that the character of "terminal diversity" presented in the declining Permian family Dvinosauridae, on the one hand, and the "archaic diversity" of a number of pioneer Early Triassic families (Tupilakosauridae, Rhytidosteidae), on the other, is in principle of the same type, expressed in the "chimeric" alternative manifestation in individual genera of alien characters of high systematic rank. The difference consists only in that within the Permian family these mosaic deviations correspond to the future (Mesozoic) generalized structural type, whereas in the later families, conversely, various variants of the retention of Paleozoic - sometimes extremely archaic - features are observed against the background of an already generally established Mesozoic organizational aspect. There is no doubt that both the "terminal" and the "archaic" manifestations of disorder (in our case belonging to different evolutionary lineages) represent simply stages of the general non-equilibrium transition from one stable organizational plan to another. If we observe such manifestations within the framework of the former plan ("senile variability"), then the question of whether to call them archaic diversity or something else depends entirely on whether an actual evolutionary transformation of this plan into some other is supposed to have occurred in this case. It may be concluded that the extinction of a living organization, as well as its historical transformation, both begin equally with an irreversible disruption of its stability. This event initiates the beginning of the search by the disrupted system for a new state of equilibrium through its reorganization by natural selection. The success of this process signifies evolutionary change; failure signifies extinction.