Developmental biology: hotspots for evolution.
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Biomedical subjects
Michael K Richardson
Publications and source records attributed to Michael K Richardson.
Developmental constraints in a comparative framework: a test case using variations in phalanx number during amniote evolution.
Constraints are factors that limit evolutionary change. A subset of constraints is developmental, and acts during embryonic development. There is some uncertainty about how to define developmental constraints, and how to formulate them as testable hypotheses. Furthermore, concepts such as constraint-breaking, universal constraints, and forbidden morphologies present some conceptual difficulties. One of our aims is to clarify these issues. After briefly reviewing current classifications of constraint, we define developmental constraints as those affecting morphogenetic processes in ontogeny. They may be generative or selective, although a clear distinction cannot always be drawn. We support the idea that statements about constraints are in fact statements about the relative frequency of particular transformations (where 'transformation' indicates a change from the ancestral condition). An important consequence of this is that the same transformation may be constrained in one developmental or phylogenetic context, but evolutionarily plastic in another. In this paper, we analyse developmental constraints within a phylogenetic framework, building on similar work by previous authors. Our approach is based on the following assumptions from the literature: (1) constraints are identified when there is a discrepancy between the observed frequency of a transformation, and its expected frequency; (2) the 'expected' distribution is derived by examining the phylogenetic distribution of the transformation and its associated selection pressures. Thus, by looking for congruence between these various phylogenetic distribution patterns, we can test hypotheses about constraint. We critically examine this approach using a test case: variation in phalanx-number in the amniote limb.
Animal Population Groups↗
Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development.
The concept of a phylotypic stage, when all vertebrate embryos show low phenotypic diversity, is an important cornerstone underlying modern developmental biology. Many theories involving patterns of development, developmental modules, mechanisms of development including developmental integration, and the action of natural selection on embryological stages have been proposed with reference to the phylotypic stage. However, the phylotypic stage has never been precisely defined, or conclusively supported or disproved by comparative quantitative data. We tested the predictions of the 'developmental hourglass' definition of the phylotypic stage quantitatively by looking at the pattern of developmental-timing variation across vertebrates as a whole and within mammals. For both datasets, the results using two different metrics were counter to the predictions of the definition: phenotypic variation between species was highest in the middle of the developmental sequence. This surprising degree of developmental character independence argues against the existence of a phylotypic stage in vertebrates. Instead, we hypothesize that numerous tightly delimited developmental modules exist during the mid-embryonic period. Further, the high level of timing changes (heterochrony) between these modules may be an important evolutionary mechanism giving rise to the diversity of vertebrates. The onus is now clearly on proponents of the phylotypic stage to present both a clear definition of it and quantitative data supporting its existence.
Animals↗
Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus).
Lamprey development is of interest to evolutionary biologists because it can inform our understanding of primitive vertebrate developmental patterns. In this study, we describe and illustrate some of the principle landmarks of organogenesis in the embryonic sea lamprey Petromyzon marinus L. at different chronological ages. We examined 63 fixed embryos spanning Piavis developmental stages 11-18+ (5-70 days postfertilization) by gross observation and histology. This period begins at late neurulation stages and ends with the formation of the larva (ammocoete). A significant difference with some previous accounts is that the anus develops not from a persistent blastopore, but by secondary canalization and proctodeum formation at the former site of the blastopore. Further, we show that the ciliated bands of the pharyngeal roof originate in the esophagus, distinguishing it from the intestine. We clarify the epithelialization of the gut, showing that the secondary gut cavity is progressively epithelialized from each end. We identify possible germ cells in the coelomic and cloacal walls. Balfour's "subnotochordal rod" is lacking in our specimens; we suggest that he may have misinterpreted the corpus adiposum. Our study is of potential value to the growing number of biologists interested in lamprey development and provides a character set that will be used : 1) in a phylogenetic study of vertebrate development, and 2) to prepare a staging series for the lamprey based on parsimony analysis.
Animals↗
Septation and separation within the outflow tract of the developing heart.
The developmental anatomy of the ventricular outlets and intrapericardial arterial trunks is a source of considerable confusion. First, major problems exist because of the multiple names and definitions used to describe this region of the heart as it develops. Second, there is no agreement on the boundaries of the described components, nor on the number of ridges or cushions to be found dividing the outflow tract, and the pattern of their fusion. Evidence is also lacking concerning the role of the fused cushions relative to that of the so-called aortopulmonary septum in separating the intrapericardial components of the great arterial trunks. In this review, we discuss the existing problems, as we see them, in the context of developmental and postnatal morphology. We concentrate, in particular, on the changes in the nature of the wall of the outflow tract, which is initially myocardial throughout its length. Key features that, thus far, do not seem to have received appropriate attention are the origin, and mode of separation, of the intrapericardial portions of the arterial trunks, and the formation of the walls of the aortic and pulmonary valvar sinuses. Also as yet undetermined is the formation of the free-standing muscular subpulmonary infundibulum, the mechanism of its separation from the aortic valvar sinuses, and its differentiation, if any, from the muscular ventricular outlet septum.
Ductus Arteriosus↗
Haeckel's ABC of evolution and development.
One of the central, unresolved controversies in biology concerns the distribution of primitive versus advanced characters at different stages of vertebrate development. This controversy has major implications for evolutionary developmental biology and phylogenetics. Ernst Haeckel addressed the issue with his Biogenetic Law, and his embryo drawings functioned as supporting data. We re-examine Haeckel's work and its significance for modern efforts to develop a rigorous comparative framework for developmental studies. Haeckel's comparative embryology was evolutionary but non-quantitative. It was based on developmental sequences, and treated heterochrony as a sequence change. It is not always clear whether he believed in recapitulation of single characters or entire stages. The Biogenetic Law is supported by several recent studies -- if applied to single characters only. Haeckel's important but overlooked alphabetical analogy of evolution and development is an advance on von Baer. Haeckel recognized the evolutionary diversity in early embryonic stages, in line with modern thinking. He did not necessarily advocate the strict form of recapitulation and terminal addition commonly attributed to him. Haeckel's much-criticized embryo drawings are important as phylogenetic hypotheses, teaching aids, and evidence for evolution. While some criticisms of the drawings are legitimate, others are more tendentious. In opposition to Haeckel and his embryo drawings, Wilhelm His made major advances towards developing a quantitative comparative embryology based on morphometrics. Unfortunately His's work in this area is largely forgotten. Despite his obvious flaws, Haeckel can be seen as the father of a sequence-based phylogenetic embryology.
Anatomy, Comparative↗
Analyzing developmental sequences within a phylogenetic framework.
Heterochrony is important as a potential mechanism of evolutionary change. However, the analysis of developmental timing data within a phylogenetic framework to identify important shifts has proven difficult. In particular, analytical problems with sequence (event) heterochrony revolve around the lack of an absolute time frame in development to allow standardization of timing data across species. An important breakthrough in this regard is the method of "event-pairing," which compares the relative timing of developmental events in a pairwise fashion. The resulting event-pair-encoded data can be mapped onto a phylogeny, which can provide important biological information. However, event-paired data are cumbersome to work with and lack a rigorous quantitative framework under which to analyze them. Critically, the otherwise advantageous relativity of event-pairing prevents an assessment of whether one or both events in a single event-pair have changed position during evolutionary history. Building on the method of event-pairing, we describe a protocol whereby event-pair transformations along a given branch are analyzed en bloc. Our method of "event-pair cracking" thereby allows developmental timing data to be analyzed quantitatively within a phylogenetic framework to infer key heterochronic shifts. We demonstrate the utility of event-pair cracking through a worked example and show how it provides a set of desired features identified by previous authors.
Animals↗
Analyzing evolutionary patterns in amniote embryonic development.
Heterochrony (differences in developmental timing between species) is a major mechanism of evolutionary change. However, the dynamic nature of development and the lack of a universal time frame makes heterochrony difficult to analyze. This has important repercussions in any developmental study that compares patterns of morphogenesis and gene expression across species. We describe a method that makes it possible to quantify timing shifts in embryonic development and to map their evolutionary history. By removing a direct dependence on traditional staging series, through the use of a relative time frame, it allows the analysis of developmental sequences across species boundaries. Applying our method to published data on vertebrate development, we identified clear patterns of heterochrony. For example, an early onset of various heart characters occurs throughout amniote evolution. This suggests that advanced (precocious) heart development arose in evolutionary history before endothermy. Our approach can be adapted to analyze other forms of comparative dynamic data, including patterns of developmental gene expression.
Age Factors↗
Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper.
The forelimb of whales and dolphins is a flipper that shows hyperphalangy (numerous finger bones). Hyperphalangy is also present in marine reptiles, including ichthyosaurs and plesiosaurs. The developmental basis of hyper-phalangy is unclear. Kükenthal suggested that phalanx anlagen split into three pieces during cetacean development, thereby multiplying the ancestral number. Alternatively, Holder suggested that apical ectodermal ridge (AER)-directed limb outgrowth might be prolonged by a timing shift (heterochrony), leading to terminal addition of extra phalanges. We prepared a series of whole mounted and serially sectioned embryonic flipper buds of the spotted dolphin Stenella attenuata. This cetacean shows marked hyperphalangy on digits II and III. We confirm previous reports that the proximodistal laying down of phalanges is prolonged in digits II and III. Histology showed that the apical ectoderm was thickened into a cap. There was a weak ridge-like structure in some embryos. The cap or ridge formed part of a bud-like mass that persisted on digits II and III at stages when it had disappeared from other digits. Thus the dolphin differs from other mammals in showing a second period of limb outgrowth during which localized hyperphalangy develops. New phalanges only formed at the tip of the digits. These findings are consistent with a model in which heterochrony leads to the terminal addition of new phalanges. Our results are more easily reconciled with the progress zone model than one in which the AER is involved in the expansion of a prepattern. We suggest that patterning mechanisms with a temporal component (i.e., the "progress zone" mechanism) are potential targets for heterochrony during limb evolution.
Animals↗