Study Of Heterochrony Research Articles

Connecting the Dots: Anatomical Network Analysis in Morphological EvoDevo

Morphological EvoDevo is a field of biological inquiry in which explicit relations between evolutionary patterns and growth or morphogenetic processes are made. Historically, morphological EvoDevo results from the coming together of several traditions, notably Naturphilosophie, embryology, the study of heterochrony, and developmental constraints. A special feature binding different approaches to morphological EvoDevo is the use of formalisms and mathematical models. Here we will introduce anatomical network analysis, a new approach centered on connectivity patterns formed by anatomical parts, with its own concepts and tools specifically designed for the study of morphological EvoDevo questions. Riedl’s concept of burden is tightly related to the use of anatomical networks, providing a nexus between the evolutionary patterns and the structural constraints that shape them.

Heterocronía y variación morfológica en anuros

Heterochrony is a concept referred to ontogenetic variation and is frequently used in comparative morphology. It involves single traits, the whole organism, size, shape and has implicit the timing in which an ontogenetic trajectory occurs. The study of heterochrony has produced terms, definitions and models in which sometimes the heterochronic variation overlaps with its morphological results and evolutionary processes. Herein, the revision of some of these terms and definitions is discussed with data of developmental variation in anurans.

Early embryogenesis in discoglossoid frogs: a study of heterochrony at different taxonomic levels

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Morphodynamic Perspectives on Convergence between the Feet and Limbs of Sauropods and Humans: Two Cases of Hypermorphosis

Only two vertebrate groups, humans and sauropod dinosaurs, have a well-developed entaxonic foot (with the big toe, or digit I, the largest), and both have vertical limbs. Thus, convergence applies not only to the feet but also to the limbs. When viewed in relation to their closest relatives among the hominoids and saurischian dinosaurs, and in the context of known developmental growth patterns in higher vertebrates, both humans and sauropod dinosaurs appear to be excellent examples of peramorphosis (specifically hypermorphosis). Thus, it is essential to understand morphodynamics as a field that is inseparable from the study of heterochrony. The morphodynamic developmental perspective, while recognized as important in genetics and embryology, has for many generations been overlooked in studies of feet, footprints and limbs (i.e., the marco-morphology of organs). Investigating these dynamics reveals striking recursive (or fractal) patterns of anterior-posterior and proximal distal development, which in turn demonstrate that vertebrate growth proceeds in an organized or “formal” manner. Thus, convergence is not merely, or only, a by-product of functional adaptation to the external environment but also a manifestation of the complex but intelligible internal organization of dynamic organic systems.

Cranial modularity and sequence heterochrony in mammals

Heterochrony, the temporal shifting of developmental events relative to each other, requires a degree of autonomy among those processes or structures. Modularity, the division of larger structures or processes into autonomous sets of internally integrated units, is often discussed in relation to the concept of heterochrony. However, the relationship between the developmental modules derived from studies of heterochrony and evolutionary modules, which should be of adaptive importance and relate to the genotype-phenotype map, has not been explicitly studied. I analyzed a series of sectioned and whole cleared-and-stained embryological and neonatal specimens, supplemented with published ontogenetic data, to test the hypothesis that bones within the same phenotypic modules, as determined by morphometric analysis, are developmentally integrated and will display coordinated heterochronic shifts across taxa. Modularity was analyzed in cranial bone ossification sequences of 12 therian mammals. A dataset of 12-18 developmental events was used to assess if modularity in developmental sequences corresponds to six phenotypic modules, derived from a recent morphometric analysis of cranial modularity in mammals. Kendall's tau was used to measure rank correlations, with randomization tests for significance. If modularity in developmental sequences corresponds to observed phenotypic modules, bones within a single phenotypic module should show integration of developmental timing, maintaining the same timing of ossification relative to each other, despite differences in overall ossification sequences across taxa. Analyses did not find any significant conservation of developmental timing within the six phenotypic modules, meaning that bones that are highly integrated in adult morphology are not significantly integrated in developmental timing.

Intraspecific heterochrony and life history evolution: decoupling somatic and sexual development in a facultatively paedomorphic salamander.

Morphological features such as size and shape are the most common focus in studies of heterochronic change. Frequently, these easily observed and measured features are treated as a major target of selection, potentially ignoring traits more closely related to fitness. We question the primacy of morphological data in studies of heterochrony, and instead suggest that principal sources of fitness, such as life history characteristics, are not only the chief targets of selection, but changes in them may necessitate changes in other (subordinate) elements of the organism. We use an experimental approach to investigate the timing of metamorphosis and maturation in a facultatively paedomorphic salamander, Ambystoma talpoideum. We determine that individuals possessing the well-known paedomorphic phenotype are peramorphic with regard to maturation, through the process of predisplacement (an earlier onset of maturation). Combining the well studied ecology of dimorphic A. talpoideum populations with theories of heterochronic mechanisms and life history evolution, we conclude that age at maturation is the principal target of selection and that morphological changes are secondary effects. Increased attention to the intimate connection between life history evolution and heterochrony is the most promising route to a better understanding of both.

Heterochrony and allometry: the analysis of evolutionary change in ontogeny.

The connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one-to-one correspondence. These relationships and outline links between different analytical frameworks are discussed.

Heterochrony and allometry: the analysis of evolutionary change in ontogeny

ABSTRACTThe connection between development and evolution has become the focus of an increasing amount of research in recent years, and heterochrony has long been a key concept in this relation. Heterochrony is defined as evolutionary change in rates and timing of developmental processes; the dimension of time is therefore an essential part in studies of heterochrony. Over the past two decades, evolutionary biologists have used several methodological frameworks to analyse heterochrony, which differ substantially in the way they characterize evolutionary changes in ontogenies and in the resulting classification, although they mostly use the same terms. This review examines how these methods compare ancestral and descendant ontogenies, emphasizing their differences and the potential for contradictory results from analyses using different frameworks. One of the two principal methods uses a clock as a graphical display for comparisons of size, shape and age at a particular ontogenic stage, whereas the other characterizes a developmental process by its time of onset, rate, and time of cessation. The literature on human heterochrony provides particularly clear examples of how these differences produce apparent contradictions when applied to the same problem. Developmental biologists recently have extended the concept of heterochrony to the earliest stages of development and have applied it at the cellular and molecular scale. This extension brought considerations of developmental mechanisms and genetics into the study of heterochrony, which previously was based primarily on phenomenological characterizations of morphological change in ontogeny. Allometry is the pattern of covariation among several morphological traits or between measures of size and shape; unlike heterochrony, allometry does not deal with time explicitly. Two main approaches to the study of allometry are distinguished, which differ in the way they characterize organismal form. One approach defines shape as proportions among measurements, based on considerations of geometric similarity, whereas the other focuses on the covariation among measurements in ontogeny and evolution. Both are related conceptually and through the use of similar algebra. In addition, there are close connections between heterochrony and changes in allometric growth trajectories, although there is no one‐to‐one correspondence. These relationships and outline links between different analytical frameworks are discussed.

The effects of muscular dystrophy on craniofacial growth in mice: a study of heterochrony and ontogenetic allometry.

Mechanical loading of muscles on bones at their sites of attachment can regulate skeletal morphology. The present study examined the effects of muscle degeneration on craniofacial growth, using two strains of muscular dystrophic mice, Mus musculus, differing in pathological severity. We collected radiographic and weight data longitudinally and digitized radiographs to obtain distances between anatomical landmarks in different functional regions of the skull. We then quantified heterochronic and allometric differences among genotypes and between sexes. Because growth is nonlinear with respect to time, we first used the Gompertz model to obtain heterochronic growth parameters, which were then tested with ANOVA. Ontogenetic allometric analyses examined the scaling relationships between various measurements with linear regressions. For most measurements the severely dystrophic mice are significantly smaller in final size than both the control and the mildly dystrophic mice, which are statistically indistinguishable. Measures of total growth and the neurocranium exhibit more differences among groups in heterochronic parameters of early ontogeny because growth in these regions is controlled primarily by brain expansion that ceases early in development. In contrast, the face and mandible exhibit more differences in later growth parameters possibly because of the increased influence of muscles on these regions as growth progresses. The severely dystrophic mice have flatter, more elongate skulls and mandibles than those of the other two genotypes, concurrent with an absence of muscular forces to stimulate growth in a superior-inferior direction.

Heterochrony and heterotopy: stability and innovation in the evolution of form

Heterochrony, change in developmental rate and timing, is widely recognized as an agent of evolutionary change. Heterotopy, evolutionary change in spatial patterning of development, is less widely known or understood. Although Haeckel coined the term as a complement to heterochrony in 1866, few studies have detected heterotopy or even considered the possibility that it might play a role in morphological evolution. We here review the roles of heterochrony and heterotopy in evolution and discuss how they can be detected. Heterochrony is of interest in part because it can produce novelties constrained along ancestral ontogenies, and hence result in parallelism between ontogeny and phylogeny. Heterotopy can produce new morphologies along trajectories different from those that generated the forms of ancestors. We argue that the study of heterochrony has been bound to an analytical formalism that virtually precludes the recognition of heterotopy, so we provide a new framework for the construction of ontogenetic trajectories and illustrate their analysis in a phylogenetic context. The study of development of form needs tools that capture not only rates of development but the space in which the changes are manifest. The framework outlined here provides tools applicable to both. When appropriate tools are used and the necessary steps are taken, a more comprehensive interpretation of evolutionary change in development becomes possible. We suspect that there will be very few cases of change solely in developmental rate and timing or change solely in spatial patterning; most ontogenies evolve by changes of spatiotemporal pattern.

MOLECULAR HETEROCHRONY IN THE PATTERN OF FIBRONECTIN EXPRESSION DURING GASTRULATION IN AMPHIBIANS.

Heterochrony is an evolutionary concept referring to changes in the relative timing of developmental events. Studies of heterochrony have concentrated mostly on morphology (e.g., Alberch and Alberch 1981; Emerson 1986). Because these studies examine heterochrony in the morphogenesis of adult structures, they deal with later aspects of development. A review of heterochrony by Raff and Wray (1989) stressed the lack of heterochronic studies of early (those stages in vertebrates from fertilization through neurulation), and especially molecular, aspects of development. One of the few exceptions involves differences in the timing of expression of three different epitopes (the antigenic determinants msp 130, Meso 1, and SP12) among different species of sea urchins (Wray and McClay 1989). While studies of molecular heterochrony are not new, they are infrequent (Raffet al. 1984; Parks et al. 1988; Wray and McClay 1989). Much as comparative studies on morphological aspects of early development reveal interspecific variability (Ballard 1981; Elinson 1987; del Pino 1989; Raff et al. 1991), molecular heterochronic studies demonstrate that early development is also varied at the level of molecular expression (Raff et al. 1991). A valuable system in which to study molecular heterochrony during early development is the expression of extracellular-matrix molecules on the blastocoel roof during gastrulation. This extracellular matrix is complex and consists of many different molecules, only some of which have

HETEROCHRONY AND ALLOMETRY: LESSONS FROM THE WATER STRIDER GENUS LIMNOPORUS.

Heterochrony and allometry both deal with evolutionary modifications of ontogenies. Although data about both morphology and age are required to identify heterochronic processes, age data are not needed to study allometry. Using a simple graphical model, we show that allometric patterns cannot be used to infer the underlying heterochronic processes. We present a case study of the water strider genus Limnoporus Stål (Heteroptera: Gerridae) to illuminate the distinct roles that allometry and heterochrony play in integrated studies of the evolution of form. Multivariate analyses reveal several evolutionary modifications of growth trajectories (changes in direction, lateral transposition, and ontogenetic scaling), which are fairly consistent with the hypothesized phylogeny of the genus. Because there is no positive correlation between instar durations and size increments, size cannot be used as a proxy for age data in studies of heterochrony. In fact, a measure of overall size itself shows a remarkable variety of heterochronic changes among the six species. Mixtures of several heterochronic processes predominate over the more unitary reflections of "pure" processes. Heterochronic changes in different branches of the phylogeny, apparently independent of size scaling, suggest considerable potential for adaptive evolution. "Local" differentiation of ontogenetic traits within small clades may be at least as important as "global" evolutionary trends in large clades and will often be missed in "global" analyses.

Experimental heterochrony in hydractiniid hydroids: Why mechanisms matter

AbstractAs with most clonal organisms, hydractiniid hydroids display a range of morphological variation from sheet‐like to runner‐like forms. Life history differences correlate with these morphological traits, exhibiting patterns commonly found in studies of heterochrony. Experimental studies of two hydractiniid species show that both morphological and life history heterochronies correlate with patterns of gastrovascular circulation. Similar experimental perturbations of energy metabolism, however, have opposite heterochronic effects on the two species. Treatment with 2,4‐dinitrophenol, an uncoupler of oxidative phosphorylation, produced diminished peripheral circulation and sheet‐like peramorphic morphologies in the runner‐like species, Podocoryne carnea. In contrast, similar manipulations of the sheet‐like species, Hydractinia symbiolongicarpus, produced variable peripheral circulation and more runner‐like, juvenilized morphologies. These results diverge at the level of morphological and life history pattern, but are consistent when viewed in terms of the physiology of the gastrovascular system. Interpretations of patterns of heterochrony must focus on the physiological and developmental mechanisms which mediate the expression of heterochronic traits.

Morphological variation in a colonial marine hydroid: a comparison of size-based and age-based heterochrony

In studies of heterochrony, timing of development is generally measured relative to some intrinsic dimension, usually size, which serves as a proxy for time. A complementary approach is to measure timing relative to chronological time, an extrinsic dimension. Here, colony growth of a marine hydroid, Hydractinia echinata, is used to compare size- and age-based approaches to rate heterochronies. Colonies consist of feeding polyps; a basal, encrusting mat; and, in some cases, stolons which extend from the mat. Size is measured by the area covered by the mat and, if present, the stolons. Rate of polyp production was compared between colonies using clonal replicates grown in a common environment. Age-based comparisons employed polyp specific growth rates calculated over the same ontogenetic time interval for each replicate. Specific growth rates for colony area were also calculated; rates-ratios (polyp/area) provided size-based measures of polyp growth, analogous to allometric coefficients commonly used in studies of rate heterochronies. These comparisons show that size can be a misleading referent for between-colony comparisons because the rate of areal growth is not constant among colonies. Size-based measures of changes in developmental rates may provide insight into patterns, but not necessarily processes, of heterochrony. The implications of the pattern-oriented framework of size-based heterochrony should be considered in paleontological studies.

HETEROCHRONOUS CHANGES AMONG AUSTRALIAN LEPTODACTYLID FROGS

This investigation has been carried out in order to estimate the extent to which osteological differences normally used as a basis for generic distinction among certain anurans may be explained on the basis of heterochronous changes in bone formation. Representative species of fourteen Australian genera of the family Leptodactylidae were compared, and an osteological survey was carried out on alizarin transparencies of sexually mature and juvenile specimens. As a basis for description, a little known and somewhat neotenic Western Australian anuran, Glauertia russelli Loveridge, was selected.Bone, as a tissue, is a useful index of heterochronous change. It gives a clear indication of the extent to which the developmental processes leading to its formation have proceeded. It often provides a reliable guide to the degree of general development attained by the time an animal reaches sexual maturity.The study of heterochrony indicates the evolutionary importance of this phenomenon in the establishment of certain species and genera. Skeletal distinctions among the Australian Leptodactylidae are readily explained, even at the generic level, in terms of such time‐axis or heterochronous changes. These, through shortening or lengthening the time of development of particular bones, or by altering the speed of their ossification, lead to differences of phylogenetic significance. The fact that not only individual variations but also specific and generic distinctions may arise in this way in certain groups of animals has an important bearing on problems of their distribution.