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.     

A new evolutionary scenario for the vertebrate jaw

The jaw is one of the earliest innovations in vertebrate history. Several recent findings suggest a scenario for jaw evolution as a progression of changes in pharyngeal developmental mechanisms. The lamprey, an extant jawless vertebrate, constitutes a model for the pre-gnathostome ancestry. Comparing expression patterns of regulatory genes between the gnathostome and lamprey embryos may enable us to get a glimpse of the essential changes that were responsible for the evolution of the jaw. We hypothesize that a specific topographical change of inductive tissue interactions to be described here brought about the jaw as an evolutionary novelty.     

Altered timing of the extracellular-matrix-mediated epithelial-mesenchymal interaction that initiates mandibular skeletogenesis in three inbred strains of mice: development, heterochrony, and evolutionary change in morphology

Subtle changes in embryonic development are a source of significant morphological alterations during evolution. The mammalian mandibular skeleton, which originates from the cranial neural crest, is a complex structure comprising several components that interact late in embryogenesis to produce a single functional unit. It provides a model system in which individual developmental events at the basis of population-level evolutionary change can be investigated experimentally. Inbred mouse strains exhibit obvious morphological differences despite the relatively short time since their divergence from one another. Some of these differences can be traced to small changes in the timing of early developmental events such as the formation of the cellular condensations that initiate skeletogenesis. This paper examines an even earlier event for changes in timing, the epithelial-mesenchymal interaction(s) required to initiate chondrogenesis of Meckel's cartilage and osteogenesis of the dentary bone. Using three inbred strains of mice (CBA, C3H and C57) we found that, within each strain, cartilage and bone are induced at the same time and by the same (mandibular) epithelium, that chondrogenesis and osteogenesis are initiated by a matrix-mediated epithelial-mesenchymal interaction, and that timing of the interactions differs among the three inbred strains. These results are discussed with respect to the possible molecular basis of such temporal shifts in inductive interactions and how such studies can be used to shed light on heterochrony as a mechanism of evolutionary change in morphology.     

Cephalic neural crest cells and the evolution of craniofacial structures in vertebrates: morphological and embryological significance of the premandibular-mandibular boundary

The vertebrate head characteristically has two types of mesenchyme: the neural crest-derived ectomesenchyme and the mesoderm derived mesenchyme. Conserved patterns of development in various animal taxa imply the presence of shared inductive events for cephalic mesenchyme. These developmental programs can serve as developmental constraints that emerge as morphological homology of embryonic patterns. To understand the evolutionary changes in the developmental programs that shape the skull, we need to separate ancestral and derived patterns of vertebrate craniogenesis. This review deals with the terminology for neural crest cell subpopulations at each developmental stage, based on the topographical relationships and possible mechanisms for specification. The aim is to identify the changes that could have occurred in the evolutionary history of vertebrates. From comparisons of a lamprey species, Lethenteron japonicum, with gnathostomes it is clear that the initial distribution of cephalic crest cells is identical in the two animal lineages. In all vertebrate embryos, the trigeminal crest (TC) cells of an early pharyngula are subdivided into three subpopulations. At this stage, only the posterior subpopulation of the TC cells is specified as the mandibular arch, as compared to the more rostral components, the 'premandibular crest cells'. Later in development, the local specification patterns of the lamprey and the gnathostomes differ, so that homology cannot be established in the craniofacial primordia, including the oral apparatus. Therefore, embryological terminology should reflect these hierarchical patterns in developmental stages and phylogeny.     

Evolutionary conservation and variability of the mesoderm development in spiralia: A peculiar pattern of nereid polychaetes

An analysis of the comparative-morphological, molecular-genetic, and evolutionary aspects of the teloblastic mesoderm formation in the Spiralia representatives was performed. The conservative and the most expressive varying features of morphogenesis and genetic developmental programs of the mesodermal germ layer were considered. Using nereid polychaetes, we revealed peculiarities of their developmental patterns, related to the role of inductive interactions and the dynamics of the molecular profile in the formation of mesodermal derivatives.     

Germline development in amniotes: A paradigm shift in primordial germ cell specification

In the field of germline development in amniote vertebrates, primordial germ cell (PGC) specification in birds and reptiles remains controversial. Avians are believed to adopt a predetermination or maternal specification mode of PGC formation, contrary to an inductive mode employed by mammals and, supposedly, reptiles. Here, we revisit and review some key aspects of PGC development that channelled the current subdivision, and challenge the position of birds and reptiles as well as the ‘binary’ evolutionary model of PGC development in vertebrates. We propose an alternative view on PGC specification where germ plasm plays a role in laying the foundation for the formation of PGC precursors (pPGC), but not necessarily of PGCs. Moreover, inductive mechanisms may be necessary for the transition from pPGCs to PGCs. Within this framework, the implementation of data from birds and reptiles could provide new insights on the evolution of PGC specification in amniotes.     

The role of inductive effect in the determination of protein structure

The inductive theory, formally introduced by G. N. Lewis has thus far found its major applications in interpreting and predicting equilibrium and kinetic properties of small organic molecules. Evidence is presented demonstrating that the inductive effect can also help to explain the determination of protein structure by its amino acid sequence. Suggestions are also made that the inductive effect plays a significant role in protein conformation changes brought about by ligand binding.     

On predictions and laws in biological evolution: Is biology able to formulate general laws and develop inductive predictions as in physics or chemistry?

Biology has so far had difficulties formulating general laws akin to physics and chemistry. Evolution and its propensity to reduce entropy could become a start for such laws in biology. Subject Categories: Evolution & Ecology, History & Philosophy of Science

Science uses evidence‐based inductive reasoning to build theories, principles, and laws. A common type of inductive reasoning is generalization, that is, projecting conclusions drawn from one or a few case studies onto a broader context. The reliability of generalizations depends upon the representativeness and the formal validation of the selected case studies, which is usually performed by hypothesis testing. Another usual type of inductive reasoning is prediction, which uses observations to develop general principles and laws that can predict or anticipate future outcomes. The reliability of these predictions is confirmed by the accomplishment of the anticipated situation. It is interesting to note that generalizations are based on the analysis of empirical evidence, whereas predictions are formulated before the desired empirical evidence, which is actually the target of the prediction, is available.

… generalizations are based on the analysis of empirical evidence, whereas predictions are formulated before the desired empirical evidence, which is actually the target of the prediction, is available.

The American philosopher of science Peter Lipton (2005) commented that we are commonly more impressed by predictions than by accommodations, as he called hypothesis testing. To illustrate this, Lipton used the discovery of Halley''s Comet. In 1705, the British astronomer Edmond Halley proposed that the comets observed in 1531, 1607, and 1682 were actually the same comet with a periodic elliptical orbit. Back then, his hypothesis did not have much impact within the scientific community. However, when Halley''s prediction was confirmed in 1758 by the return of the comet, the intellectual world in Europe widely accepted the existence of a single comet, which was subsequently named Halley''s Comet. Halley''s prediction may seem straightforward, even trivial, considering the characteristic periodicity of 75 years in previous observations. Yet, it was the predictive success, rather than prior observations, that convinced the scientific community of his conclusion.Physics is considered one of the strongest branches of science—along with chemistry and mathematics—in regard to the generality and accuracy of its predictions. Biology seems still to be in its infancy, and the search for regularities that could lend to potential generalizations is the most common approach (Dodds, 2009). This is due in part to the high level of complexity of the living world, its evolutionary change over time, and its relationships with the environment. As emphasized by the German evolutionary biologist Ernst Mayr (2004), these intrinsic and unique features of living beings, which are intimately associated with the genetic code, clearly differentiate biology from other natural sciences and make the fundamental laws of physics and chemistry insufficient to understand the living world.The main aim of this essay is to discuss whether biological research is able to develop inductive predictions similar to physics or chemistry. First, I present some classical examples of physical and chemical discoveries based on inductive predictions, such as the Higgs boson, interstellar dark matter, and the periodic table of elements. As all these advances are based on the previous existence of fundamental laws, the question arises whether similar laws exist in biology to support physics‐like inductive predictions. I suggest that, if these laws exist, they should emerge from the evolutionary process, which is the main biological singularity. Thus, it should be possible to make inductive predictions based on the fossil record, which is the fundamental evolutionary evidence. Indeed, it seems that the lack of evolutionary laws is the main drawback for inductive prediction in studying evolution, which cannot escape to Lipton’s accommodation procedures, that is, hypothesis testing and generalization.

Physics is considered one of the strongest branches of science – along with chemistry and mathematics – in regard to the generality and accuracy of its predictions.

     

Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss

We address the developmental and evolutionary mechanisms underlying fore- and hindlimb development and progressive hindlimb reduction and skeletal loss in whales and evaluate whether the genetic, developmental, and evolutionary mechanisms thought to be responsible for limb loss in snakes "explain" loss of the hindlimbs in whales. Limb loss and concurrent morphological and physiological changes associated with the transition from land to water are discussed within the context of the current whale phylogeny. Emphasis is placed on fore- and hindlimb development, how the forelimbs transformed into flippers, and how the hindlimbs regressed, leaving either no elements or vestigial skeletal elements. Hindlimbs likely began to regress only after the ancestors of whales entered the aquatic environment: Hindlimb function was co-opted by the undulatory vertical axial locomotion made possible by the newly evolved caudal flukes. Loss of the hindlimbs was associated with elongation of the body during the transition from land to water. Limblessness in most snakes is also associated with adoption of a new (burrowing) lifestyle and was driven by developmental changes associated with elongation of the body. Parallels between adaptation to burrowing or to the aquatic environment reflect structural and functional changes associated with the switch to axial locomotion. Because they are more fully studied and to determine whether hindlimb loss in lineages that are not closely related could result from similar genetically controlled developmental pathways, we discuss developmental (cellular and genetic) processes that may have driven limb loss in snakes and leg-less lizards and compare these processes to the loss of hindlimbs in whales. In neither group does ontogenetic or phylogenetic limb reduction result from failure to initiate limb development. In both groups limb loss results from arrested development at the limb bud stage, as a result of inability to maintain necessary inductive tissue interactions and enhanced cell death over that seen in limbed tetrapods. An evolutionary change in Hox gene expression--as occurs in snakes--or in Hox gene regulation--as occurs in some limbless mutants--is unlikely to have initiated loss of the hindlimbs in cetaceans. Selective pressures acting on a wide range of developmental processes and adult traits other than the limbs are likely to have driven the loss of hindlimbs in whales.     

What is menstruation for? On the projectibility of functional predicates in menstruation research

In 1993, biologist Margie Profet captured the attention of the popular press with the publication of her radical thesis: menstruation has a function. Traditional theories, she claims, typically view menstruation as a functionless by-product of cyclic flux. The details of Profet’s functional account are similarly radical: she argues that menstruation has been naturally selected to defend the female reproductive tract from sperm-borne pathogens. There are a number of weaknesses in Profet’s evolutionary analysis. However, I focus on a set of pragmatic problems that arise prior to any details of her evolutionary account. In arguing for the importance of pragmatic considerations, I draw from the linguistic analyses of Nelson Goodman. I conclude that critical investigation of the evolutionary details of Profet’s pathogen defense account will be more feasible if and when biologists more frequently feature the female system of pathogen defense in their inductive generalisations. The system needs to be better entrenched before its functional components, such as menstruation, can be thoroughly investigated.     

Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH

The transition from vegetative to reproductive development establishes new growth patterns required for flowering. This switch is controlled by environmental and/or intrinsic developmental cues that converge at the shoot apical meristem (SAM). During this developmental transition, floral inductive signals cause the vegetative meristem to undergo morphological changes that are essential for flowering. Arabidopsis plants containing null mutations in two paralogous BEL1-like (BELL) homeobox genes, PENNYWISE (PNY) and POUND-FOOLISH (PNF), disrupt the transition from vegetative to reproductive development. These double mutants are completely unable to flower even though the SAM displays morphological and molecular changes that are consistent with having received floral inductive signals. These studies establish a link between the competence to receive floral inductive signals and restructuring of the SAM during floral evocation.     

Mechanisms of germ cell specification across the metazoans: epigenesis and preformation

Germ cells play a unique role in gamete production, heredity and evolution. Therefore, to understand the mechanisms that specify germ cells is a central challenge in developmental and evolutionary biology. Data from model organisms show that germ cells can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis). Here we review existing data on 28 metazoan phyla, which indicate that although preformation is seen in most model organisms, it is actually the less prevalent mode of germ cell specification, and that epigenetic germ cell specification may be ancestral to the Metazoa.     

Mechanisms driving neural crest induction and migration in the zebrafish and Xenopus laevis

The neural crest is an evolutionary adaptation, with roots in the formation of mesoderm. Modification of neural crest behavior has been is critical for the evolutionary diversification of the vertebrates and defects in neural crest underlie a range of human birth defects. There has been a tremendous increase in our knowledge of the molecular, cellular, and inductive interactions that converge on defining the neural crest and determining its behavior. While there is a temptation to look for simple models to explain neural crest behavior, the reality is that the system is complex in its circuitry. In this review, our goal is to identify the broad features of neural crest origins (developmentally) and migration (cellularly) using data from the zebrafish (teleost) and Xenopus laevis (tetrapod amphibian) in order to illuminate where general mechanisms appear to be in play, and equally importantly, where disparities in experimental results suggest areas of profitable study.     

Evo-Devo: evolutionary developmental mechanisms

Evolutionary developmental biology (Evo-Devo) as a discipline is concerned, among other things, with discovering and understanding the role of changes in developmental mechanisms in the evolutionary origin of aspects of the phenotype. In a very real sense, Evo-Devo opens the black box between genotype and phenotype, or more properly, phenotypes as multiple life history stages arise in many organisms from a single genotype. Changes in the timing or positioning of an aspect of development in a descendant relative to an ancestor (heterochrony and heterotopy) were two evolutionary developmental mechanisms identified by Ernst Haeckel in the 1870s. Many more have since been identified, in large part because of our enhanced understanding of development and because new mechanisms emerge as development proceeds: the transfer from maternal to zygotic genomic control; cell-to-cell interactions; cell differentiation and cell migration; embryonic inductions; functional interactions at the tissue and organ levels; growth. Within these emergent processes, gene networks and gene cascades (genetic modules) link the genotype with morphogenetic units (cellular modules, namely germ layers, embryonic fields or cellular condensations), while epigenetic processes such as embryonic inductions, tissue interactions and functional integration, link morphogenetic units to the phenotype. Evolutionary developmental mechanisms also include interactions between individuals of the same species, individuals of different species, and species and their biotic and/or abiotic environment. Such interactions link ecological communities. Importantly, there is little to distinguish the causality that underlies these interactions from that which underlies inductive interactions within embryos.     

Behavioural changes and the adaptive diversification of pigeons and doves

What factors determine the extent of evolutionary diversification remains a major question in evolutionary biology. Behavioural changes have long been suggested to be a major driver of phenotypic diversification by exposing animals to new selective pressures. Nevertheless, the role of behaviour in evolution remains controversial because behavioural changes can also retard evolutionary change by hiding genetic variation from selection. In the present study, we apply recently implemented Ornstein–Uhlenbeck evolutionary models to show that behavioural changes led to associated evolutionary responses in functionally relevant morphological traits of pigeons and doves (Columbiformes). Specifically, changes from terrestrial to arboreal foraging behaviour reconstructed in a set of phylogenies brought associated shorter tarsi and longer tails, consistent with functional predictions. Interestingly, the transition to arboreality accelerated the rates of evolutionary divergence, leading to an increased morphological specialization that seems to have subsequently constrained reversals to terrestrial foraging. Altogether, our results support the view that behaviour may drive evolutionary diversification, but they also highlight that its evolutionary consequences largely depend on the limits imposed by the functional demands of the adaptive zone.     

Chronological changes in the sucrase antigen-inducing activity and development of the regional identity in the intestinal mesoderm of the chick embryo

Developmental changes in mesodermal activity to induce intestine-like differentiation expressing sucrase antigen in the endoderm and changes in endodermal reactivity to such an activity in the digestive tract of the chick embryo were analyzed. Digestive-tract endoderms of embryos at 3 days of incubation were highly responsive to the inductive effect of the 5 day duodenal mesenchyme, with the stomach endoderm lying nearest to the intestine having the highest reactivity. Endodermal reactivity decreased with increasing age. It was almost absent in the endoderm of the esophagus or proventriculus of 6 day embryos and in the endoderm of the gizzard of 7 day embryos. The activity of the mesoderm to induce intestine-like differentiation in 5 day gizzard endoderm was high in the 5–10 day duodenal mesenchyme, but was rarely found in 14 day duodenal mesenchyme. This activity was specific to intestinal mesenchymes, among which the duodenal mesenchyme had the highest activity in 5 day embryos. The 3 day intestinal mesenchyme may already have the inductive activity. The presumptive intestinal mesoderm of 1.5 day embryos seemed to have a slight or no activity, but it may have intestinal identity and may manifest a high inductive activity later.