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.     

An integrative approach identifies developmental sequence heterochronies in freshwater basommatophoran snails

Adopting an integrative approach to the study of sequence heterochrony, we compared the timing of developmental events encompassing a mixture of developmental stages and functional traits in the embryos of 12 species of basommatophoran snails in an explicit phylogenetic framework. PARSIMOV analysis demonstrated clear functional heterochronies associated both with basal branches within the phylogeny and with terminal speciation events. A consensus of changes inferred under both accelerated transformation and delayed transformation optimizations identified four heterochronies where the direction of movement was known plus six twin heterochronies where the relative movements of the two events could not be assigned. On average, 0.5 and 0.58 events were inferred to have changed their position in the developmental sequence on internal and terminal branches of the phylogeny, respectively; these values are comparable with frequencies of sequence heterochrony reported in mammals. Directional heterochronies such as the early occurrence of body flexing in relation to the ontogeny of the eye spots, heart beat, and free swimming events occurred convergently and/or at different levels (i.e., familial, generic, and species) within the phylogeny. Such a functional approach to the study of developmental sequences has highlighted the possibility that heterochrony may have played a prominent role in the evolution of this group of invertebrates.     

Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony

Developmental biology often yields data in a temporal context. Temporal data in phylogenetic systematics has important uses in the field of evolutionary developmental biology and, in general, comparative biology. The evolution of temporal sequences, specifically developmental sequences, has proven difficult to examine due to the highly variable temporal progression of development. Issues concerning the analysis of temporal sequences and problems with current methods of analysis are discussed. We present here an algorithm to infer ancestral temporal sequences, quantify sequence heterochronies, and estimate pseudoreplicate consensus support for sequence changes using Parsimov-based genetic inference [PGi]. Real temporal developmental sequence data sets are used to compare PGi with currently used approaches, and PGi is shown to be the most efficient, accurate, and practical method to examine biological data and infer ancestral states on a phylogeny. The method is also expandable to address further issues in developmental evolution, namely modularity.     

From Haeckel to event-pairing: the evolution of developmental sequences

Summary Development involves a series of developmental events, separated by transformations, that follow a particular order or developmental sequence. The sequence may in turn be arbitrarily subdivided into contiguous segments (developmental stages). We discuss the properties of developmental sequences. We also examine the differing analytical approaches that have been used to analyse developmental sequences in an evolutionary context. Ernst Haeckel was a pioneer in this field. His approach was evolutionary and he introduced the idea of sequence heterochrony (evolutionary changes in the sequence of developmental events). Despite the availability of detailed developmental data (e.g. Franz Keibel’s ‘Normal Tables’), Haeckel was unable to undertake a quantitative analysis of developmental data. This is now possible through computer-based analytical techniques such as event-pairing, which can extract important biological information from developmental sequences by mapping them onto established phylogenies. It may also yield data that can be used in phylogeny reconstruction, although the inherent ‘non-independence’ of the data may make this invalid. In future, the methods discussed here may be applied to the analysis of patterns of gene expression in embryos, or adapted to studying gene order on chromosomes.     

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.     

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.     

Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.     

The ontogeny of the lower reproductive tract of the landsnail Helix aspersa (Gastropoda: Mollusca)

We provide a size-based ontogenetic sequence of the development and differentiation of the lower reproductive tract of the heterobranch gastropod Helix aspersa (Müller 1774). Twelve development stages distributed among nine size classes were recognized based on readily visible changes in morphology and changes in tissue density. Geometric morphometrics was used to calculate the deformation between stages as represented by thin-plate spline bending energies. The developmental stages and sequence of developmental events are also compared to previously published scenarios for the evolution of stylommatophoran and other pulmonate reproductive tracts. These comparisons suggest that heterochronies, which include both acceleration and retardation, are operating in the morphological evolution of the pulmonate lower reproductive tract. This supports previous observations that largest number of developmental changes coincides with the transition to sexual maturity, which is also seen in the exponential curve of bending energies we observed in Helix aspersa. The belated organogenesis makes the ontogeny of the complex hermaphroditic reproductive system of pulmonates readily observable in size-friendly juveniles. This observation, coupled with the ease of raising individuals in the laboratory, recommends Helix aspersa as a potential model laboratory system for investigating molluscan evolutionary development.     

Sequence heterochrony and the evolution of development

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.     

Assessing the phylogenetic utility of sequence heterochrony: evolution of avian ossification sequences as a case study

The evolution of developmental sequences, or sequence heterochrony, is an emerging field of study that addresses the temporal interplay between evolution and development. Some phylogenetic signal has been found in developmental sequence data, but sampling has generally been limited to small numbers of taxa and few developmental events. Here we present the largest ossification sequence dataset to date. The sequences are composed of ossification events throughout the avian skeleton, and are used to address the evolutionary signal of ossification sequence data within this clade. The results indicate that ossification sequences are conserved in birds, and show a stronger phylogenetic signal than previous studies, perhaps due to the volume of data. Phylogenetic signal is not strong enough, however, to consider ossification sequence data to be any better at resolving phylogenetic hypotheses than other morphological data and just as prone to evolutionary convergence. There is no one-to-one correlation between ossification sequence and developmental stage. We discuss some methodological implications of our findings, as well as commonalities in avian ossification sequences such as early ossification of the long bones relative to the dermatocranium, and of the hindlimb over the forelimb.     

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.     

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.     

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.     

Phylogeny-based developmental analyses illuminate evolution of inflorescence architectures in dogwoods (Cornus s. l., Cornaceae)

? Inflorescence architecture is important to angiosperm reproduction, but our knowledge of the developmental basis underlying the evolution of inflorescence architectures is limited. Using a phylogeny-based comparative analysis of developmental pathways, we tested the long-standing hypothesis that umbel evolved from elongated inflorescences by suppression of inflorescence branches, while head evolved from umbels by suppression of pedicels. ? The developmental pathways of six species of Cornus producing different inflorescence types were characterized by scanning electron microscopy (SEM) and histological analysis. Critical developmental events were traced over the molecular phylogeny to identify evolutionary changes leading to the formation of umbels and heads using methods accounting for evolutionary time and phylogenetic uncertainty. ? We defined 24 developmental events describing the developmental progression of the different inflorescence types. The evolutionary transition from paniculate cymes to umbels and heads required alterations of seven developmental events occurring at different evolutionary times. ? Our results indicate that heads and umbels evolved independently in Cornus from elongated forms via an umbellate dichasium ancestor and this process involved several independent changes. Our findings shed novel insights into head and umbel evolution concealed by outer morphology. Our work illustrates the importance of combining developmental and phylogenetic data to better define morphological evolutionary processes.     

Cranial Suture Closure Patterns in Sciuridae: Heterochrony and Modularity

Studies of sequence heterochrony in mammalian evolution have revealed differences in bone ossification between and within major clades. Sequences of late stage developmental events have been less well studied, and the relation of modularity to sequence heterochrony at these stages has not been explicitly tested. Here, the first data on cranial suture closure are provided for members of Sciuridae. Sequence heterochrony is quantified using the recently developed Parsimov-based genetic inference (PGi) algorithm to identify shifts in suture closure sequence, and modularity in heterochronic shifts is tested. Results indicate that suture closure pattern was quite variable among sciurids, and interspecific correspondence in closure sequence was generally lower than has been found for other rodents, and for carnivorans. A number of sequence heterochronies were detected for inclusive clades, and these were not randomly distributed but mainly concentrated among sutures that exhibited high rank variability and belonged to the orbit and cranial vault modules, suggesting that some regions of the cranium exhibited a greater capacity for variation in suture closure. Heterchronies were not detected for sutures belonging to the basicranium, or anterior orbit-nasal modules, both of which are recognized as highly integrated modules based on landmark data. Modularity of suture closure sequence was not significant for any modules following multiple-comparison correction, which contrasts with modularity that has been recovered in early stage, ossification sequence events among other mammals.     

Progress and challenges in studies of the evolution of development

Plant evolutionary developmental genetics (EDG) has made considerable progress over the last decade. This is in part due to the accumulation of large amounts of sequence data that have provided robust organismal phylogenies and, increasingly, broad assessments of molecular evolution. Attempts to use primary sequence data to identify genes that have changed function in evolutionary time have not been as successful as initially hoped. The coding sequences of most genes, which are more amenable to statistical analysis than are regulatory sequences, are generally under purifying selection, as would be expected if much evolutionary change is the result of changes in cis-regulatory sequences. Sequence-based analysis of the regulatory sequences themselves remains difficult. Comparative studies of gene expression have been useful to identify genes whose developmental role may have changed in evolutionary time and will be critical to the future development of EDG. Such studies can be used to test hypotheses of gene function. Transformation experiments are often illuminating, but can be hard to interpret, particularly if genes from multiple species are all placed into a single heterologous system such as Arabidopsis. The ideal experiment would be a gene swap or promoter swap between two species, but this awaits development of good transformation systems. The immediate need for EDG is studies of gene expression on a massive scale, far broader than any studies undertaken to date.     

A new technique for identifying sequence heterochrony

Sequence heterochrony (changes in the order in which events occur) is a potentially important, but relatively poorly explored, mechanism for the evolution of development. In part, this is because of the inherent difficulties in inferring sequence heterochrony across species. The event-pairing method, developed independently by several workers in the mid-1990s, encodes sequences in a way that allows them to be examined in a phylogenetic framework, but the results can be difficult to interpret in terms of actual heterochronic changes. Here, we describe a new, parsimony-based method to interpret such results. For each branch of the tree, it identifies the least number of event movements (heterochronies) that will explain all the observed event-pair changes. It has the potential to find all alternative, equally parsimonious explanations, and generate a consensus, containing the movements that form part of every equally most parsimonious explanation. This new technique, which we call Parsimov, greatly increases the utility of the event-pair method for inferring instances of sequence heterochrony.     

Variation, plasticity and modularity in anuran development

Although anuran development is generally thought to be relatively conservative, a great deal of variation is evident when different species are compared. This report summarizes the results of comparative analyses of different aspects of anuran development. These include differences in sequence and timing of developmental events, the effects of genome size, and the effects of different life history strategies on anuran embryogenesis. The results show that anuran development is plastic at the evolutionary level, and many changes can occur in the developmental processes of anurans throughout their evolution. Changes are apparently rapid, and are as common as cladogenic events. This evolutionary plasticity can be attributed to the modular nature of anuran development. Different modules can shift relative to one another in time or in space, creating variations in the observed developmental patterns. However, shifts in modules can occur even without having a significant effect on the ultimate outcome of the process. I discuss the implications of the modular nature of development on the evolution of anuran development, and of the group in general.     

Time's arrow: heterochrony and the evolution of development

The concept of heterochrony, which denotes a change in the relative timing of developmental events and processes in evolution, has accompanied attempts to link evolution and development for well over a century. During this time the definition of heterochrony and the application of the concept have varied and by the late 1990's, many questioned the usefulness of the concept. However, in the past decade studies of heterochrony have been revitalized by a new focus on developmental sequence, an examination of heterochrony in explicit phylogenetic contexts and increasing tendencies to examine the heterochrony of many kinds of events, including cellular, molecular and genetic events. Examples of such studies are reviewed in this paper and it is argued that this new application of heterochrony provides an extraordinarily rich opportunity for understanding the developmental basis of evolutionary change.