Heterochronies,heterotopies, and cell resources of development in ontogenetic and evolutionary transformations

Classification and gene regulation of heterochronies and heterotopies as temporal and spatial evolutionary changes are considered. The intensity and duration of stem cell proliferation of a developing organism are connected with heterochronies and give rise to heterotopies. It is proposed that evolutionary emergence of new populations of stem cells (local embryomorphosis) is connected with heterotopies and heterochronies of gene expression, which support cell proliferation and temporarily suppress differentiation. The concept of modularity of evolutionary developmental biology and the theory of reproductive strategy naturally supplement each other and provide a better understanding of some ontogenetic changes in evolution. Developmental, morphological, and functional features of nematodes and vertebrates display alternative evolutionary trends with the predominance of progenesis and neoteny, respectively.     

Process heterochronies in endochondral ossification

Heterochrony, evolutionary changes in developmental rates and timing, is a key concept in the construction of a synthesis of development and evolution. Heterochronic changes in vertebrate evolution have traditionally been identified through plesiomorphic-apomorphic comparisons of bone growth. This methodological framework assumes that observed heterochronies are the outcome of dissociations of developmental processes in time. Recent findings of non-heterochronic developmental changes underlying morphological heterochrony invalidate this assumption. In this paper, a function for bone growth (at the organ level) has been mathematically deduced from the underlying developmental mechanisms. The temporal domain of the model spans from the time at maximum growth rate, after the formation of growth plates, to the time at atrophy of the proliferating stratum of cells. Three organizational levels were considered: (a) cell kinetics of endochondral ossification, (b) variation of bone growth rates and (c) variation of accumulated bone growth with increasing age. This quantitative model provides an excellent tool to deal with the problem of the developmental basis of morphological change. I have modelled potential evolutionary changes on the system at different levels of biological organization. This new framework involves an epistemological shift in heterochronic analysis from a pattern-oriented inductive way to a process-oriented deductive way. The analysis of the relationships between the evolutionary alterations of endochondral ossification and the morphological expression of these changes reveals that observed pattern heterochronies can be the outcome of different process heterochronies. Moreover, I discuss at length the heteroposic hypothesis, that evolutionary changes in the tight regulation of the amount of protein synthesized by a cell population during development would underlie acceleration or deceleration in cases of evolutionary changes in the initial number of proliferating cells at growth plates. Future research on the genetic basis of process heterochronies and heteroposies will complete our understanding of these evolutionary phenomena.     

Experimental approach to the hypotheses of heterochronic evolution in lower vertebrates

Heterochronies, temporal changes in ancestral ontogeny, are proposed to play the major role in microand macroevolutionary transformations of lower vertebrates. However, the evolutionary role of heterochronies often remains hypothetical, not verified experimentally. In the present paper, participation of heterochronies in (1) the origin of lacustrine fish species flocks, (2) the diversification of skeletal morphology in teleosts, and (3) the skull evolution in amphibians is experimentally verified. For this purpose, the temporal parameters of ontogeny were directly changed via artificial alterations of the thyroid hormones level in different representatives of lower vertebrates. The data obtained indicate that heterochronies are among the main mechanisms responsible for the current morphological diversity displayed by lower vertebrates at different phylogenetic levels.     

Morphological evolution: Estimation principles, patterns, and mechanisms

Directions, modes, specializations, and coordination systems of morphofunctional changes are discussed based on modern data. Phylogenetic heterochronies (pedomorphoses and outstripping), which provide the basis for parallel, mosaic, and saltation development and different rates of morphological evolution, are regarded as important events of morphological diversification. The analysis of specificity and relationships of structural levels of organization (including genetic and epigenetic) and the elaboration of evolutionary principles of their dynamic stability are thought to be the most promising fields of modern research.     

The problem of the skin derivatives' origin in the amniote evolution. The skin appendages--scale, feather, and hair

Overview of modern data on morphology of the skin derivatives in the higher vertebrates is given. Analysis of convergent similarities between the hair and feathers themselves as well as between their follicles makes it possible to forward a "generative" concept of the evolutionary origin of various ecto-mesodermal derivatives, such as keratinized dermal appendages (scales, feathers, hair). This concept appeared as a result of the author's studies on the skin derivatives, as well as of the data on molecular biology and the tissue engineering showing similar mechanisms of morphogenesis of the dermal appendages. Recurrently published ideas on various heterochronies in generations of the skin derivatives both in the onto- and the phylogeneses are also taken into acount. Various dermal appendages have appeared in the evolution of the higher vertebrates as independent generations of the ecto- and mesodermal tissues. Their parallel origin was caused by similar changes in the metabolism and molecular regulation of morphogenesis.     

Evolution of ontogeny and nature of heterochronies

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.     

Methods for the analysis of developmental sequence data

SUMMARY Heterochrony, evolutionary changes in developmental timing, can be studied either by examining changes in growth or changes in the sequence of developmental events. Developmental sequence data has the potential to address many important questions in the field of developmental evolution, but methodological challenges remain due to the biological and logical dependence of events in a ranked sequence. In the past 10 years, the study of sequence heterochrony has undergone a rebirth, with the creation of several new methods for the analysis of this type of data. These methods can be divided into two broad categories: phenetic comparisons between terminal taxa that strive to uncover integrations within the developmental sequences and putative shared sequence heterochronies, and phylogeny-based methods that derive ancestor-descendent sequence heterochronies and establish statements of sequence evolution. In this review, we will discuss the strengths and weaknesses of the methodologies that have been proposed to quantitatively examine developmental sequence data, and studies that have attempted to implement them in an evolutionary context.     

MORPHOMETRICS AND CLADISTICS: MEASURING PHYLOGENY IN THE SEA URCHIN ECHINOCARDIUM

A phylogenetic approach to the study of evolutionary patterns is based on taxic homologies (synapomorphies). In contrast, the recognition of evolutionary processes (namely heterochronies) involves analysis of the entire morphology. Recent developments in geometric morphometry permit analysis of morphological similarities grounded in operational homologies. Such morphometric techniques are explored (1) at the level of evolutionary processes, and (2) as a complement in exploration of phylogenetic relationships. To examplify this, we perform a two-part study of the ontogeny and phylogeny of the spatangoid sea urchin Echinocardium. First, a phylogenetic analysis of ten Recent species in the genus is performed on 18 informative characters of the test. Second, morphological divergences among the species are analyzed using procrustean (superimposition) methods based on 49 homologous points. An additive distance tree is built from a matrix of morphometric distances among adult specimens. This tree is fully congruent with the phyletic results. Ontogenetic processes are explored by inserting ontogenetic series into the analysis. A distance tree including the juvenile stages shows that the general evolutionary trend of the genus is peramorphic, but species-to-species comparisons attest that no general clinal trend exists. Our analysis emphasizes the importance of morphometric approaches in evolutionary studies (1) for the understanding of heterochronies; (2) to trace the morphological implications of phylogenetic patterns; and (3) to estimate the impact of homoplasies.     

De Novo Evolution of Complex, Global and Hierarchical Gene Regulatory Mechanisms

Gene regulatory networks exhibit complex, hierarchical features such as global regulation and network motifs. There is much debate about whether the evolutionary origins of such features are the results of adaptation, or the by-products of non-adaptive processes of DNA replication. The lack of availability of gene regulatory networks of ancestor species on evolutionary timescales makes this a particularly difficult problem to resolve. Digital organisms, however, can be used to provide a complete evolutionary record of lineages. We use a biologically realistic evolutionary model that includes gene expression, regulation, metabolism and biosynthesis, to investigate the evolution of complex function in gene regulatory networks. We discover that: (i) network architecture and complexity evolve in response to environmental complexity, (ii) global gene regulation is selected for in complex environments, (iii) complex, inter-connected, hierarchical structures evolve in stages, with energy regulation preceding stress responses, and stress responses preceding growth rate adaptations and (iv) robustness of evolved models to mutations depends on hierarchical level: energy regulation and stress responses tend not to be robust to mutations, whereas growth rate adaptations are more robust and non-lethal when mutated. These results highlight the adaptive and incremental evolution of complex biological networks, and the value and potential of studying realistic in silico evolutionary systems as a way of understanding living systems.     

EVOLUTIONARY LOSS OF LARVAL FEEDING: DEVELOPMENT,FORM AND FUNCTION IN A FACULTATIVELY FEEDING LARVA,BRISASTER LATIFRONS

Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.     

Role of heterochronies in the morphogenesis of paleozoic ammonoids

Various types of evolutionary changes related to shifts in the appearance or order of formation of characters, i.e., heterochronies are shown. The most common such changes in Paleozoic ammonoids was the appearance of mosaic forms combining conservative and advanced characters resulting from recapitulation and paedomorphosis. These phenomena are related to certain phylogenetic stages in each group: the growth stage predominantly showed recapitulations; the diversification stage showed the appearance of many mosaic forms; the decline stage commonly shows paedomorphosis connected with retardation.     

The morphofunctional approach in paleontology

The principle of actualism is regarded as the major principle in morphofunctional studies of fossil organisms, which is based on comparisons of evolutionary series of both extinct and extant taxa. The objects and specificity of morphofunctional studies in paleontology are discussed. The revelation of relationships between morphological and functional archetypes are considered to be the major task of these studies. The ecosystem approach, constrains on actualistic reconstruction imposed by various morphofunctional modi, hierarchy of functions at different levels of structural organization and at different phylogenetic stages are considered. It is shown that parallel development and the mosaic pattern of characters are accounted for by general morphogenetic mechanisms and heterochronies.     

Transposable elements donate lineage-specific regulatory sequences to host genomes

The evolutionary implications of transposable element (TE) influences on gene regulation are explored here. An historical perspective is presented to underscore the importance of TE influences on gene regulation with respect to both the discovery of TEs and the early conceptualization of their potential impact on host genome evolution. Evidence that points to a role for TEs in host gene regulation is reviewed, and comparisons between genome sequences are used to demonstrate the fact that TEs are particularly lineage-specific components of their host genomes. Consistent with these two properties of TEs, regulatory effects and evolutionary specificity, human-mouse genome wide sequence comparisons reveal that the regulatory sequences that are contributed by TEs are exceptionally lineage specific. This suggests a particular mechanism by which TEs may drive the diversification of gene regulation between evolutionary lineages.     

Morphogenesis Rate Variability and Modularity of Development in Jurassic Ammonites of the Genus Arcticoceras Spath, 1924

The high variability of ammonites is largely due to the diversity of combinations of individual heterochronies (bradimorphy, tachymorphy, bradygeronty, and tachygeronty) and the modularity of development. Using the genus Arcticoceras as an example, it was shown that heterochronies of various directions can be combined in any number of characters, and individual heterochronies differ from phylogenetic ones by their smaller range, and a larger number of combinations. The study of such combinations allowed intraspecific morphs to be recognized, and available Arcticoceras species to be revised. During the Early and Middle Bathonian, the family Cardioceratidae evolved through a series of paedomorphosis, and after the appearance of Cadoceratinae, through accelerations.     

An apparent progressive and recurrent evolutionary restriction in tissue expression of a gene,the lactate dehydrogenase-C gene,within a family of bony fish (Salmoniformes: Umbridae)

Summary Unexpectedly large differences in the tissue patterns of lactate dehydrogenase-C (Ldh-C) gene regulation were observed among species of fish within the family Umbridae (Salmoniformes). Normally, all the species within a family or order of advanced fishes exhibit the same, tissue-restricted pattern ofl-latate dehydrogenase C₄ isozyme synthesis—either eye- or liver-restricted expression, but not both. However, within the Umbridae the more anciently derived species had a more generalized (primitive) tissue expression, whereas the more recently derived species had a more tissue-restricted expression, predominating in the eye. Given the relative divergence times among the species estimated by genetic distance (using 51 protein-coding loci), divergence from the presumed primitive expression of the Ldh-C gene appears to have been proceeding more rapidly in some species lineages than others. This narrowing of Ldh-C gene tissue regulatory specificity within the family Umbridae is similar to the general trend observed over much greater evolutionary times within the class of bony fishes. The results support the hypothesis of repeated evolutionary canalizations of Ldh-C gene regulation from the generalized tissue expression in more primitive species to a predictable tissue-restricted expression (in either eye or liver) in advanced species. Furthermore, in the Umbridae, this progressive restriction of tissue expression of isozymes has taken place during the evolution of both the Ldh-C and Ldh-B genes. These evolutionary trends in the regulation of isozyme-locus tissue expression in the bony fishes are consistent with either an intrinsically conditioned trend of change in gene regulation or with a response to natural selection.     

Darwin,the amphibians,and the natural selection

A critical review of Darwin's publications shows that he did not dissert much about amphibians, in comparison with the other tetrapods. However, in “A Naturalist's Voyage round the World”, Darwin described for the first time several amphibian species and was surprised by their peculiar way of life, terrestrial or euryhaline. These amphibian observations around the world led Darwin to discuss evolutionnary notions, like developmental heterochronies or evolving convergences, and later to illustrate his famous natural selection theory. This is confirmed, for example, by the publication of “On the Origin of Species” where Darwin ironically questioned creation theory, trying to explain the absence of amphibians on oceanic islands. Lamarck also considered amphibians as relevant material to illustrate his theory of acquired character heredity. These historical uses of lissamphibians as evolutionary models have been mostly realized before any amphibian fossil discovery, i.e. out of a palaeontological context.     

Skin derivatives in vertebrate ontogeny and phylogeny

The skin of vertebrates has numerous and diverse derivatives, either located within the epithelial sheet itself (glands) or extending above its surface (teeth, scales, feathers, hairs, etc.). Many of them have a modular structure and constitute structural-functional units. Ontogenetically, all skin derivatives are of ectomesodermal origin, and their morphogenesis is subject to metabolic control, heterochronies (divergence in the timing of origination and development), and regulation by means of tissue interactions and molecular signaling via similar pathways. The diversification (origination of morphological diversity) of skin derivatives within the same morphological type is explained by the development of new generations of ectomesodermal structures separated by heterochronies and regulated by changes in the gradients of molecular signaling pathways under the influence of environmental factors. Evolutionary relationships between the majority of skin derivatives are obscure, except for teeth and glands associated with sensory organs that have evolved together with these organs. Apparently, many vertebrate skin derivatives (scales, feathers, hairs, and glands) originated as novelties at nodal stages of phylogeny and subsequently evolved convergently or in parallel.     

Mosaic heterochrony and evolutionary modularity: the trilobite genus Zacanthopsis as a case study

Logical connections exist between evolutionary modularity and heterochrony, two unifying and structuring themes in the expanding field of evolutionary developmental biology. The former sees complex phenotypes as being made up of semi-independent units of evolutionary transformation; the latter requires such a modular organization of phenotypes to occur in a localized or mosaic fashion. This conceptual relationship is illustrated here by analyzing the evolutionary changes in the cranidial ontogeny of two related species of Cambrian trilobites. With arguments from comparative developmental genetics and functional morphology, we delineate putative evolutionary modules within the cranidium and examine patterns of evolutionary changes in ontogeny at both global and local scales. Results support a case of mosaic heterochrony, that is, a combination of local heterochronies affecting the different parts individuated in the cranidium, leading to the complex pattern of allometric repatterning observed at the global scale. Through this example, we show that recasting morphological analyses of complex phenotypes with a priori knowledge or hypotheses about their organizational and variational properties can significantly improve our interpretation and understanding of evolutionary changes among related taxa, fossil and extant. Such considerations open avenues to investigate the large-scale dynamics of modularity and its role in phenotypic evolution.     

Root hairs, trichomes and the evolution of duplicate genes

The MYB-class proteins WEREWOLF and GLABRA1 are functionally interchangeable, even though one is normally expressed solely in roots and the other only in shoots. This shows that their different functions are the result of the modification of cis-regulatory sequences over evolutionary time. The two genes thus provide an example of morphological diversification created by gene duplication and changes in regulation.