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Every aspect of biological orderliness is a result of evolution, which expresses the systemic reorganization of organismal body plan, along with the way of its ontogenetic formation. Phyletic changes in the developmental rates (heterochronies) experienced by the organism or its structures exemplify just a kind of such consequences. The current belief that heterochronies are the causes of evolutionary events is based on the assumption that evolution of ontogeny proceeds in the same way as the ontogeny itself, i.e., from a germ cell to adult state. This premise (termed here “the central dogma”) is the cornerstone of traditional ideas of the evolutionary mechanism, regardless of whether it is perceived in terms of gene mutations or “embryonic modes.” In fact, the directions of two transformations compared are opposite each other. An evolutionary change in the body plan results from reorganization of the developmental system, which comes in response to disturbance of stability of the system’s terminal (adult) state. Realized by selection, this change starts immediately from the terminal state and then spreads in generations towards early ontogenetic stages. Heterochronies show just the same dynamics of events irrespective of whether they reflect the acceleration or delay of development. Empirically, such course of evolutionary changes was grounded most evidently by Severtsov in the early version of his concept of the phylembryogenesis. The theoretical basis of the same regularity is provided by the Schmalhausen–Waddington’s theory.
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... In line with this dominating belief, the vector of evolutionary changes is directly identified with the course of ontogeny (which, in turn, inspires students to attempted restorations of evolutionary mechanisms based on the ontogenetic events). This postulate, which constitutes a kind of the "central dogma" of traditional evolutionary thinking (Shishkin, 2010(Shishkin, , 2016, may have different interpretations (see below). But in any case, by default, it assumes that the orderly correspondence between the type of germ cell and the adult organization (a property of normal ontogeny) is the only conceivable mode of relations between them, and thus it can undergo transformation only as a whole, i.e. by a leap in a course of the generation change. ...
Evolution of living systems is a succession of historical changes in their equilibrium states. In the individual life cycle, every such state is realized as an equilibrium of developmental system, i.e. as its adult organizational norm. A trigger for a switching the system to a search for a new equilibrium is the loss under critical conditions of effective regulation of normal development towards uniform final state. This is manifested by replacement of the adult norm by its individual deviations. Thus, the organizational change begins with its adult state, which is the first to undergo the disturbance under new conditions. Accordingly, with the transition of the organization to a new equilibrium, the remodeling of the developmental system extends in generations from the adult stage to earlier ones. These premises contrast with the accepted belief that evolutionary events begin with individual changes in the germ cell. The only substantiated alternative to the last approach is objectively presented by the concepts of Schmalhausen and Waddington, in which the change in systemic organization starts with stabilization of selected phenotypic variations generated by violation of the current adult norm. The evolutionary spreading of organizational changes towards the early developmental stages constitutes in this case a natural consequence of the stabilization process. This course of events is actually reflected in different ways in the many empirical generalizations that have grown in the scope of more traditional views. It may be predicted that this pattern will come to provide a basis for a revised understanding of the evolutionary process.
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The relationship between ontogeny and phylogeny (heterochrony) plays a pivotal role in evolution, forming the link between genetics and natural selection. Heterochrony can be invoked to explain much intraspecific phenotypic variation, including polymorphism and sexual dimorphism. Many interspecific examples of heterochrony demonstrate that dissociation is a common phenomenon, with some features being paedomorphic (ancestral juvenile characters present in the adult) while others are peramorphic (ancestral adult characters present in the juvenile). Selection of heterochronic morphotypes sometimes focuses on factors other than morphology. For instance, size or life history strategy might also be targeted. Extrinsic factors, such as predation pressure, play an important role in directing evolutionary trends that have been facilitated by heterochrony. -from Author
“It's not all heterochrony.” Raff (1996) “Heterochrony … explains everything.” McNamara (1997) Few evolutionary topics have generated more confusion and controversy than heterochrony. Commonly defined as “evolution via change in rate or timing of development,” heterchrony has historically become associated with genocidal ideologies, simple-minded theories of evolution, and a bloated, baroque jargon describing patterns produced by largely unknown mechanisms. With a track record like that, perhaps the most surprising aspect of heterochrony is its continued, even rapid, growth as an area of productive scientific inquiry. For example, the number of papers devoted to heterochronic topics continues to increase in many evolutionary journals and books (reviews in Reilly et al. 1997; Klingenberg 1998), including those devoted to human development (Bogin 1997) and evolution (Vrba 1998; McKinney 1998; Parker and McKinney 1999).
The controversy concerning the value of ontogenicdata for phylogenetic reconstruction is briefly reviewed. Examples to illustrate the problem are presented from data concerning plethodontid salamanders, and include an analysis of ontogenetic trajectories in the genus Batrachoseps and modifications of early ontogeny in bolitoglossine salamenders. Some workers advocate using ontogenetic data to establish the polarity of characters that vary among taxa. This view is rejected. The entire ontogeny of a character is the focus of interest, for ontogenies evolve as wholes and any part is subject to change. Only outgroup analysis is of value in determining character polarity, and ontogenetic data alone can be misleading. Nevertheless, examples presented show that ontogenetic information can serve as the basis for the establishment of hypotheses concerning the history of groups and can provide insight into evolutionary dynamics.
SYNOPSIS. The role of development in constraining the directionality and patterns of morphological evolution is examined. The nature of morphological variation and appearance of morphological novelties is determined by the epigenetic properties of the organism. Consideration of these properties has profound implications for current theories of morphological evolution. Developmental constraints impose severe limitations on the gradualistic action of directional selection. Evolutionis viewed as the result of differential survival of morphological novelties. However, the production of morphological novelties by developmental programs is not random. This non-randomness in morphologically expressed genetic mutations-an epigenetic property-can result in phyletic trends, parallelisms and convergences.
The concept of heterochrony has long had a central place in evolutionary theory. During their long history, heterochrony and several associated concepts such as paedomorphosis and neoteny have often been contentious and they continue to be criticized. Despite these criticisms, we review many examples showing that heterochrony and its associated concepts are increasingly cited and used in many areas of evolutionary study. Furthermore, major strides are being made in our understanding of the underlying genetic and developmental mechanisms of heterochrony, and in the methods used to describe heterochronic changes. A general theme of this accumulating research is that some of the simplistic notions of heterochrony, such as terminal addition, simple rate genes, and “pure” heterochronic categories are invalid. However, this research also shows that a more sophisticated view of the hierarchical nature of heterochrony provides many useful insights and improves our understanding of how ontogenetic changes are translated into phylogenetic changes.
Consideration of the ways in which ontogenetic development may be modified to give morphological novelty provides a conceptual framework that can greatly assist in formulating and testing hypotheses of patterns and constraints in evolution. Previous attempts to identify distinct modes of ontogenetic modification have been inconsistent or ambiguous in definition, and incomprehensive in description of interspecific morphological differences. This has resulted in a situation whereby almost all morphological evolution is attributed to heterochrony, and the remainder is commonly either assigned to vague or potentially overly inclusive alternative classes, or overlooked altogether. The present paper recognizes six distinct modes of ontogenetic change, each a unique modification to morphological development: (1) rate modification, (2) timing modification, (3) heterotopy, (4) heterotypy, (5) heterometry, and (6) allometric repatterning. Heterochrony, modeled in terms of shape/time/size ontogenetic parameters, relates to parallelism between ontogenetic and phylogenetic shape change and results from a rate or timing modification to the ancestral trajectory of ontogenetic shape change. Loss of a particular morphological feature may be described in terms of timing modification (extreme postdisplacement) or heterometry, depending on the temporal development of the feature in the ancestor. Testing hypotheses of the operation of each mode entails examining the morphological development of the ancestor and descendant by using trajectory-based studies of ontogenetically dynamic features and non-trajectory-based studies of ontogenetically static features. The modes identified here unite cases based on commonalities of observed modification to the process of morphological development at the structural scale. They may be heterogeneous or partially overlapping with regard to changes to genetic and cellular processes guiding development, which therefore require separate treatment and terminology. Consideration of the modes outlined here will provide a balanced framework within which questions of evolutionary change and constraint within phylogenetic lineages can be addressed more meaningfully.
The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized. 2001 The Linnean Society of London ADDITIONAL KEY WORDS: development – craniofacial – mammal – marsupial.
While a framework and terminology for heterochrony has been referenced widely in the literature and appears to be accepted by nearly all workers in the field we have found it to be a confusing and incomplete model that has led to varying degrees of misunderstanding about heterochrony among evolutionary biologists. Much of the confusion exists because the model is explicitly limited to phylogenetic patterns (interspecific comparisons), but has been used for intraspecific comparisons. Because heterochrony may underlie all morphological variation and possibly is the developmental phenomenon producing all morphological change it is important that descriptions of heterochronic patterns and processes be clear and precise over all levels of analysis. To this end we discuss and clarify the previous model for heterochrony, reject some of the terminology and suggest alternatives, and then expand the model to include a new nomenclature for intraspecific heterochronic phenomena. Our modifications are essential to maintain the critical conceptual distinction between inter- vs. intraspecific heterochronic patterns and processes in evolutionary biology.
The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.
In natural sciences, the advance of evolutionary thought and growth of empirical knowledge are not strictly correlated. The
state of theory primarily tends to be controlled by a mode of collective thinking that historically dominates a given branch
of science. This particularly holds true for the natural selection concept, which has two alternative interpretations known
as the genetic and epigenetic theories of evolution. The final result of their competition, albeit predictable, will not be
based upon any kind of “crucial evidence” giving advantage to either of them. The above result will be in fact attained as
soon as the evolutionary biology can overcome the tradition of mosaic thinking which enables the incompatible concepts to
be combined. In this respect, the key point to be realized is that the idea of corpuscular determination of the ontogeny is
incompatible with understanding the development as a systemically controlled process.
Abstract. -We present a quantitative method for describing how heterochronic changes in ontogeny relate to phyletic trends. This is a step towards creating a unified view of developmental biology and evolu- tionary ecology in the study of morphological evolution. Using this ...
Some systematists, pattern cladists in particular, have recently argued that phylogenetic patterns are essentially a reflection
of the “orderliness of ontogeny.” In fact, these authors contend that information derived from the study of ontogenetic sequences
is the most reliable source to determine character polarities. Heterochronic analysis, in spite of its emphasis on process
over pattern, shares many of the same assumptions about ontogeny. This is because both systematic and heterochronic analyses
belong to the comparative tradition of embryology. Essentially, ontogeny is viewed as a sequence of morphological stages that
are assumed to be conserved. Furthermore, in spite of claims that the analyses are based on Von Baer's law, the approach is
fundamentally Haeckelian, since its comparison of ontogenies (at least in the manner currently done in systematics and heterochrony)
requires that embryonic stages be homologized with adult stages. Nelson's revised “biogenetic law” is used as an example to
illustrate these points. The nature and informational value of ontogenetic sequences are examined and I conclude that, in
contrast with strictly temporal sequences, the only “meaningful” sequences (in the sense that they will be conserved through
phylogeny) are the causal ones, where the antecedent stage is required for the expression of the subsequent one. However,
I present some examples of causal sequences where inductive relationships change through phylogeny. Therefore, there are no
good arguments to assume a priori that ontogenetic sequences are conserved. A more fundamental problem is pointed out when
I discuss that the methodology of comparison of ontogenetic sequences, used by systematists and heterochronists, is not compatible
with the dynamic perspective of development endorsed by experimental and mechanistically-oriented embryologists. Examples
are provided where, although the process can be arranged in a sequence of stages, these are effectively meaningless and useless
in a systematic context. Two additional empirical cases are discussed where a heterochronic analysis is integrated within
a dynamical framework of development. A paradox emerges, since the resultant morphology in the derived species is not represented
in the primitive (“ancestral”) ontogenetic sequence, in spite of the fact that it has been produced by a regulation in the
timing and developmental rates of the ancestral ontogeny. I conclude that these problems result from the usage of a static
and unrealistic view of ontogeny. A major challenge in systematics will be to incorporate the dynamic perspective of development
into a methodological framework amenable to comparative analysis. I agree with Nelson and others in that development is ordered
and that this internal order structures pattern. However, the information is not necessarily in the ontogenetic sequence.
Heterochrony has become a central organizing concept relating development and evolution. Unfortunately, the standard definition of heterochrony--evolutionary change in the rate or timing of developmental processes--is so broad as to apply to any case of phenotypic evolution. Conversely, the standard classes of heterochrony only accurately describe a small subset of the possible ways that ontogeny can change. I demonstrate here that the nomenclature of heterochrony is meaningful only when there is a uniform change in the rate or timing of some ontogenetic process, with no change in the internal structure of that process. Given two ontogenetic trajectories, we can test for this restricted definition of heterochrony by asking if a uniform stretching or translation of one trajectory along the time axis superimposes it on the other trajectory. If so, then the trajectories are related by a uniform change in the rate or timing of development. If not, then there has been change within the ontogenetic process under study. I apply this technique to published data on fossil Echinoids and to the comparison of human and chimpanzee growth curves. For the Echinoids, some characters do show heterochrony (hypermorphosis), while others, which had previously been seen as examples of heterochrony, fail the test--implying that their evolution involved changes in the process of development, not just the rate at which it proceeded. Analysis of human and chimpanzee growth curves indicates a combination of neoteny and sequential hypermorphosis, two processes previously seen as alternate explanations for the differences between these species.
One of the most persistent questions in comparative developmental biology concerns whether there are general rules by which ontogeny and phylogeny are related. Answering this question requires conceptual and analytic approaches that allow biologists to examine a wide range of developmental events in well-structured phylogenetic contexts. For evolutionary biologists, one of the most dominant approaches to comparative developmental biology has centered around the concept of heterochrony. However, in recent years the focus of studies of heterochrony largely has been limited to one aspect, changes in size and shape. I argue that this focus has restricted the kinds of questions that have been asked about the patterns of developmental change in phylogeny, which has narrowed our ability to address some of the most fundamental questions about development and evolution. Here I contrast the approaches of growth heterochrony with a broader view of heterochrony that concentrates on changes in developmental sequence. I discuss a general approach to sequence heterochrony and summarize newly emerging methods to analyze a variety of kinds of developmental change in explicit phylogenetic contexts. Finally, I summarize a series of studies on the evolution of development in mammals that use these new approaches.
The present crisis of evolutionism was predictable initially, since the preformational model of development expressed in the idea of discrete heredity contradicts the systemic properties of ontogenesis. Correspondingly, the principle of selection of inherited factors cannot explain evolution. The synthetic theory based on this principle contains insoluble contradictions in its key notions. According to the alternative epigenetic theory based on the integrity of living organization, heredity is a product of selection and expresses teleonomic direction of development to a stable final state. Unification of the genetic concept of evolution with recognition of the integrity of development is principally impossible. The cause of dominance of genetic views on evolution consists in the correspondence of the mechanistic tradition of the 18-19th centuries, rather than in their logistic substantiation. For the same reason, the biology as a whole is characterized by identification of specific linear dependences with the laws of evolution. Following this path in search for "new evolutionary synthesis" invites a priori its failure. Evolutionary interpretation of genetic generalizations is only possible on the basis of their description in terms of development.