Test of Von Baer's law of the conservation of early development

One of the oldest and most pervasive ideas in comparative embryology is the perceived evolutionary conservation of early ontogeny relative to late ontogeny. Karl Von Baer first noted the similarity of early ontogeny across taxa, and Ernst Haeckel and Charles Darwin gave evolutionary interpretation to this phenomenon. In spite of a resurgence of interest in comparative embryology and the development of mechanistic explanations for Von Baer's law, the pattern itself has been largely untested. Here, I use statistical phylogenetic approaches to show that Von Baer's law is an unnecessarily complex explanation of the patterns of ontogenetic timing in several clades of vertebrates. Von Baer's law suggests a positive correlation between ontogenetic time and amount of evolutionary change. I compare ranked position in ontogeny to frequency of evolutionary change in rank for developmental events and find that these measures are not correlated, thus failing to support Von Baer's model. An alternative model that postulates that small changes in ontogenetic rank are evolutionarily easier than large changes is tentatively supported.     

In search of the vertebrate phylotypic stage: a molecular examination of the developmental hourglass model and von Baer's third law

In 1828, Karl von Baer proposed a set of four evolutionary "laws" pertaining to embryological development. According to von Baer's third law, young embryos from different species are relatively undifferentiated and resemble one another but as development proceeds, distinguishing features of the species begin to appear and embryos of different species progressively diverge from one another. An expansion of this law, called "the hourglass model," has been proposed independently by Denis Duboule and Rudolf Raff in the 1990s. According to the hourglass model, ontogeny is characterized by a starting point at which different taxa differ markedly from one another, followed by a stage of reduced intertaxonomic variability (the phylotypic stage), and ending in a von-Baer-like progressive divergence among the taxa. A possible "translation" of the hourglass model into molecular terminology would suggest that orthologs expressed in stages described by the tapered part of the hourglass should resemble one another more than orthologs expressed in the expansive parts that precede or succeed the phylotypic stage. We tested this hypothesis using 1,585 mouse genes expressed during 26 embryonic stages, and their human orthologs. Evolutionary divergence was estimated at different embryonic stages by calculating pairwise distances between corresponding orthologous proteins from mouse and human. Two independent datasets were used. One dataset contained genes that are expressed solely in a single developmental stage; the second was made of genes expressed at different developmental stages. In the second dataset the genes were classified according to their earliest stage of expression. We fitted second order polynomials to the two datasets. The two polynomials displayed minima as expected from the hourglass model. The molecular results suggest, albeit weakly, that a phylotypic stage (or period) indeed exists. Its temporal location, sometimes between the first-somites stage and the formation of the posterior neuropore, was in approximate agreement with the morphologically defined phylotypic stage. The molecular evidence for the later parts of the hourglass model, i.e., for von Baer's third law, was stronger than that for the earlier parts.     

Hypothesis testing in evolutionary developmental biology: a case study from insect wings

Developmental data have the potential to give novel insights into morphological evolution. Because developmental data are time-consuming to obtain, support for hypotheses often rests on data from only a few distantly related species. Similarities between these distantly related species are parsimoniously inferred to represent ancestral aspects of development. However, with limited taxon sampling, ancestral similarities in developmental patterning can be difficult to distinguish from similarities that result from convergent co-option of developmental networks, which appears to be common in developmental evolution. Using a case study from insect wings, we discuss how these competing explanations for similarity can be evaluated. Two kinds of developmental data have recently been used to support the hypothesis that insect wings evolved by modification of limb branches that were present in ancestral arthropods. This support rests on the assumption that aspects of wing development in Drosophila, including similarities to crustacean epipod patterning, are ancestral for winged insects. Testing this assumption requires comparisons of wing development in Drosophila and other winged insects. Here we review data that bear on this assumption, including new data on the functions of wingless and decapentaplegic during appendage allocation in the red flour beetle Tribolium castaneum.     

Why the short face? Developmental disintegration of the neurocranium drives convergent evolution in neotropical electric fishes

Convergent evolution is widely viewed as strong evidence for the influence of natural selection on the origin of phenotypic design. However, the emerging evo‐devo synthesis has highlighted other processes that may bias and direct phenotypic evolution in the presence of environmental and genetic variation. Developmental biases on the production of phenotypic variation may channel the evolution of convergent forms by limiting the range of phenotypes produced during ontogeny. Here, we study the evolution and convergence of brachycephalic and dolichocephalic skull shapes among 133 species of Neotropical electric fishes (Gymnotiformes: Teleostei) and identify potential developmental biases on phenotypic evolution. We plot the ontogenetic trajectories of neurocranial phenotypes in 17 species and document developmental modularity between the face and braincase regions of the skull. We recover a significant relationship between developmental covariation and relative skull length and a significant relationship between developmental covariation and ontogenetic disparity. We demonstrate that modularity and integration bias the production of phenotypes along the brachycephalic and dolichocephalic skull axis and contribute to multiple, independent evolutionary transformations to highly brachycephalic and dolichocephalic skull morphologies.     

Developmental selection and self-organization

Developmental selection is the differential survival and proliferation of developmental units, such as cellular lineages. This type of internal selection has been proposed as an explanation for diverse examples of self-organization, from the wiring of brains to the formation of pores on leaf surfaces. A general understanding of developmental selection has been slowed by failure to understand its relationship to familiar forms of genetical selection and evolution. I show the formal analogies between models of developmental selection and genetical selection. The general method I outline for the analysis of selective systems partitions self-organizing selective systems into generative rules that create variation and selective filters that move the population toward a target design. The method also emphasizes aggregate statistical measures of evolving systems, such as the covariance between particular traits and fitness. The identification of useful aggregate measures is a crucial step in the analysis of selective systems. I apply these concepts to a model of self-organization in ant colonies.     

Ontogenetic changes in the carapace shape of the non-marine ostracod Eucypris virens (Jurine)

Developmental changes in carapace form (size+shape) during ontogeny have been explored in Eucypris virens (Crustacea, Ostracoda) using elliptic Fourier analysis. Clones from different geographic localities raised under controlled constant conditions (temperature and photoperiod) were used to characterize developmental pathways in the species. A larger data set including field populations and laboratory populations cultured under a range of environmental conditions were used to infer influence of environmental factors on carapace shape changes during ontogeny. Size changes between consecutive juvenile stages support empirical laws describing the doubling of ostracod volume at each moult. Ontogenetic changes point out the remarkable influence of environmental conditions on carapace shape.     

Ontogeny–a way forward for systematics, a way backward for phylogeny

In the history of biology, the term 'evolution' has carried a dual meaning, viz. ontogeny (the unfolding of the germ) versus phylogeny (descent with modification). A problem in modern biology is the question of whether it is ontogeny which creates phylogeny, or whether it is phylogeny which moulds ontogeny. The paper explores the relationship of ontogeny to phylogeny in the context of 'pattern cladism'. The conclusion is that the analysis of ontogeny provides a direct method for classification ('a way forward for systematics'), which is a logical prerequisite for a phylogenetic interpretation of ontogenetic sequences ('a way backward for phylogeny'). The ontogenetic process of growth, subdivision and differentiation is related to the 'morphogenetic tree theory' on the basis of Von Baer's "laws of individual development". This conceptual relation shows that ontogeny creates phylogeny in an upward direction within the morphogenetic tree, whereas phylogeny (by means of natural selection) moulds ontogeny in a downward direction. A conflict originates with the conventions of Linnaean classification if ontogenetic divergence is proposed as a causal agent in the origin of higher taxa. It is proposed to solve this conflict by viewing individual organisms (or reproductive communities) not as constituents, but as representatives of higher taxa.     

The evolution of developmental strategy in marine invertebrates

Developmental mode varies widely in most animal phyla. These differences in developmental strategy exert a profound influence on the ecology and evolution of closely related species. The mechanistic alterations in ontogeny that lead to switches in developmental mode are coming under increasing scrutiny. Echinoids are one of the best-understood groups in this regard. Parallel modifications in direct-developing echinoids point to some of the key changes in oogenesis and embryogenesis that produce switches in developmental mode.     

Quantitative tests of general models for the evolution of development

Comparative developmental biologists have proposed models to describe patterns of conserved features in vertebrate ontogeny. The hourglass model suggests evolutionary change is most difficult at an intermediate "phylotypic" stage, the adaptive penetrance model suggests change is easiest at an intermediate stage, and the early conservation model suggests change is easier later in ontogeny. Although versions of some of these models have been discussed since the nineteenth century, quantitative approaches have been proposed only recently. Here we present quantitative phylogenetic approaches to evaluating trends in the evolution of ontogeny. We apply these approaches to the proposed models and demonstrate that an existing approach to assessing these models is biased. We show that the hourglass, adaptive penetrance, and early conservation models are unnecessarily complex explanations of the patterns observed in developmental event data for 14 species of vertebrates. Rather, a simpler model that postulates that evolutionary change is easier between ontogenetically adjacent events is adequate.     

A topological look into the evolution of developmental programs

Rapid advance of experimental techniques provides an unprecedented in-depth view into complex developmental processes. Still, little is known on how the complexity of multicellular organisms evolved by elaborating developmental programs and inventing new cell types. A hurdle to understanding developmental evolution is the difficulty of even describing the intertwined network of spatiotemporal processes underlying the development of complex multicellular organisms. Nonetheless, an overview of developmental trajectories can be obtained from cell type lineage maps. Here, we propose that these lineage maps can also reveal how developmental programs evolve: the modes of evolving new cell types in an organism should be visible in its developmental trajectories and therefore in the geometry of its cell type lineage map. This idea is demonstrated using a parsimonious generative model of developmental programs, which allows us to reliably survey the universe of all possible programs and examine their topological features. We find that, contrary to belief, tree-like lineage maps are rare, and lineage maps of complex multicellular organisms are likely to be directed acyclic graphs in which multiple developmental routes can converge on the same cell type. Although cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs that produce low-functioning organisms. Our model indicates that additionally, lineage map topologies are correlated with such a functional property: the ability of organisms to regenerate.     

Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body.

The cloning, characterization and developmental expression patterns of two novel murine Hox genes, Hox-4.6 and Hox-4.7, are reported. Structural data allow us to classify the four Hox-4 genes located in the most upstream (5') position in the HOX-4 complex as members of a large family of homeogenes related to the Drosophila homeotic gene Abdominal B (AbdB). It therefore appears that these vertebrate genes are derived from a selective amplification of an ancestral gene which gave rise, during evolution, to the most posterior of the insect homeotic genes so far described. In agreement with the structural colinearity, these genes have very posteriorly restricted expression profiles. In addition, their developmental expression is temporally regulated according to a cranio-caudal sequence which parallels the physical ordering of these genes along the chromosome. We discuss the phylogenetic alternative in the evolution of genetic complexity by amplifying either genes or regulatory sequences, as exemplified by this system in the mouse and Drosophila. Furthermore, the possible role of 'temporal colinearity' in the ontogeny of all coelomic (metamerized) metazoans showing a temporal anteroposterior morphogenetic progression is addressed.     

The contribution of developmental palaeontology to extensions of evolutionary theory

Evo‐devo is featuring prominently in current discussion to extend evolutionary theory. Developmental palaeontology, the study of life history evolution and ontogeny in fossils, remains an area of investigation that could benefit from, but also illuminate, the discourse and research agenda of evo‐devo. Understanding how and why evolution proceeds in phenotypic space is an important goal of evo‐devo and one that can be significantly enriched through the examination of development in the fossil record (Palaeo‐evo‐devo). Such an approach permits developmental pathways to be extended into the past, constraining hypotheses of developmental evolution in ways that cannot be predicted by patterns observed from extant taxa alone. The comparison of developmental dynamics among extant and extinct taxa yields a more complete understanding of the temporal persistence of factors that shape evolution in phenotypic space. As more data are compiled that document ‘fossilized ontogenies’, a stage will emerge from which insights into the evolution of development can begin to appraise those phenotypes that are inaccessible to evo‐devo.     

How many processes are responsible for phenotypic evolution?

SUMMARY In addressing phenotypic evolution, this article reconsiders natural selection, random drift, developmental constraints, and internal selection in the new extended context of evolutionary developmental biology. The change of perspective from the "evolution of phenotypes" toward an "evolution of ontogenies" (evo-devo perspective) affects the reciprocal relationships among these different processes. Random drift and natural selection are sibling processes: two forms of post-productional sorting among alternative developmental trajectories, the former random, the latter nonrandom. Developmental constraint is a compound concept; it contains even some forms of natural ("external" and "internal") selection. A narrower definition ("reproductive constraints") is proposed. Internal selection is not a selection caused by an internal agent. It is a form of environment-independent selection depending on the level of the organism's internal developmental or functional coordination. Selection and constraints are the main deterministic processes in phenotypic evolution but they are not opposing forces. Indeed, they are continuously interacting processes of evolutionary change, but with different roles that should not be confused.     

The morphological and ontogenetic changes in the Protozoa during the transition to a sessile mode of life

The morphological adaptations of protozoans to sessile mode life and evolutionary changes in ontogeny are considered. There are main morphotypes of sessile protists: stalked organisms that attached to substrate by the extended base of body (basal disk), and unstalked organisms that are flatted on substrate. The origin of the morphotypes was independent in different taxa and involved nonhomologous structures. Adaptation to the sessile mode of life in the protists was connected with the progressive increase in the body size and intensity of organelle functions by polymerisation, subsequent division of function and change of functions. Evolution of adhesive organelles is characterised by growing intensity of their functions by allometric growth (usually without polymerisation), and in some cases with the subsequent division of functions and change of functions. The evolution manifests itself primarily in the organelles that provide interaction of cell with environment. The organelles that ensuring functioning of cell change due to correlations with the organelles of the first group. These two groups of organelles are similar to A.N. Sewertsoff's ecto- and endosomatic organs in multicellular organisms. The ontogeny of the sessile protists included three stages: formation of the migratory stage, distribution and choice of substrate and metamorphosis of the migratory stage after adhesion. As a rule there are no recapitulations on the first stage. The majority of structures tomotes or zoospores are inherited from the parent cell. Thus the present of some ancestral characteristics at the earlier stages of protistean ontogeny is display of the Baer's law. The main features of ontogeny evolution in sessile protists are the anaboly of the additional stages of life cycle, the displays of archallaxis or deviation during the migratory stage formation, and anaboly at the stage of buds morphogenesis after adhesion. At the last stage, the study of recapitulations is most perspective with the decision of phylogenetic problems in sessile protists.     

On the validity of von Baer's laws in evolutionary morphology

The validity of von Baer's "laws" on the general and the specific in vertebrate morphogenesis (especially organogenesis) was varified. The author starts from the hypothesis that the rudiments of traits newly acquired during morphogenesis are not rigid, not immovable, during morphogenesis, but that the action of protracted stabilizing selection during the geological ages causes them to spread and pushes them back to the perfected and stabilized in adulthood, thereby shortening the recapitulation of ancestral traits, which may eventually disappear below the threshold of detectable morphogenesis. On the basis of this thesis of the dynamics of evolutionary morphogenesis (the author bases his considerations on his studies of the morphogenesis of the avian carpometacarpus and the nasal apparatus in Sauropsida), the author comes to the conclusion that these von Baer's rules presuppose rigidity and immovability of phylogenetic morphogenesis. In fact, the general and the specific in evolutionary morphogenesis (especially organogenesis) is continuously motion, the general changes to the specific and the specific to the general and both categories undergo incessant changes. Von Baer's rules are thus not generally valid, they cannot rank as laws and in many cases they do not apply to morphogenesis (especially organogenesis), particularly in the transitional phase of evolutionary morphogenesis, when the rudiments of progressive evolutionary deviations have reached the early phases of morphogenesis and recapitulation has disappeared - and the "general" has also disappeared.     

Evolution of branched regulatory genetic pathways: directional selection on pleiotropic loci accelerates developmental system drift

Developmental systems are regulated by a web of interacting loci. One common and useful approach in studying the evolution of development is to focus on classes of interacting elements within these systems. Here, we use individual-based simulations to study the evolution of traits controlled by branched developmental pathways involving three loci, where one locus regulates two different traits. We examined the system under a variety of selective regimes. In the case where one branch was under stabilizing selection and the other under directional selection, we observed "developmental system drift": the trait under stabilizing selection showed little phenotypic change even though the loci underlying that trait showed considerable evolutionary divergence. This occurs because the pleiotropic locus responds to directional selection and compensatory mutants are then favored in the pathway under stabilizing selection. Though developmental system drift may be caused by other mechanisms, it seems likely that it is accelerated by the same underlying genetic mechanism as that producing the Dobzhansky-Muller incompatibilities that lead to speciation in both linear and branched pathways. We also discuss predictions of our model for developmental system drift and how different selective regimes affect probabilities of speciation in the branched pathway system.     

Modeling the evolution of regulatory elements by simultaneous detection and alignment with phylogenetic pair HMMs

The computational detection of regulatory elements in DNA is a difficult but important problem impacting our progress in understanding the complex nature of eukaryotic gene regulation. Attempts to utilize cross-species conservation for this task have been hampered both by evolutionary changes of functional sites and poor performance of general-purpose alignment programs when applied to non-coding sequence. We describe a new and flexible framework for modeling binding site evolution in multiple related genomes, based on phylogenetic pair hidden Markov models which explicitly model the gain and loss of binding sites along a phylogeny. We demonstrate the value of this framework for both the alignment of regulatory regions and the inference of precise binding-site locations within those regions. As the underlying formalism is a stochastic, generative model, it can also be used to simulate the evolution of regulatory elements. Our implementation is scalable in terms of numbers of species and sequence lengths and can produce alignments and binding-site predictions with accuracy rivaling or exceeding current systems that specialize in only alignment or only binding-site prediction. We demonstrate the validity and power of various model components on extensive simulations of realistic sequence data and apply a specific model to study Drosophila enhancers in as many as ten related genomes and in the presence of gain and loss of binding sites. Different models and modeling assumptions can be easily specified, thus providing an invaluable tool for the exploration of biological hypotheses that can drive improvements in our understanding of the mechanisms and evolution of gene regulation.     

Evidence for evolutionary changes in ontogeny: Paleontological, comparative-morphological, and molecular aspects

It has been noted that the integration of modern data of paleontology, comparative morphology, developmental biology, and molecular genetics forms the basis for understanding the mechanisms of evolutionary transformations of ontogeny. Paleontological and morphological evidence of the evolutionary changes in ontogeny are considered based on the data of cell and molecular biology and developmental genetics. It is shown that reorganizations of gene regulatory cascades (mainly Hox genes) play a key role in the evolution of the axial organization of animals and modifications of the limb structure of metazoans, whereas the formation of new types of structures was apparently determined by the emergence of new populations of stem cells in embryogenesis (for example, neural crest cells in the evolution of vertebrates).     

Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Characterizing the relationships between genotype and phenotype for developmental adaptive traits is essential to understand the evolutionary dynamics underlying biodiversity. In holometabolous insects, the time to reach the reproductive stage and pupation site preference are two such traits. Here we characterize aspects of the genetic architecture for Developmental Time (decomposed in Larval and Pupal components) and Pupation Height using lines derived from three natural populations of Drosophila melanogaster raised at two temperatures. For all traits, phenotypic differences and variation in plasticity between populations suggest adaptation to the original thermal regimes. However, high variability within populations shows that selection does not exhaust genetic variance for these traits. This could be partly explained by local adaptation, environmental heterogeneity and modifications in the genetic architecture of traits according to environment and ontogenetic stage. Indeed, our results show that the genetic factors affecting Developmental Time and Pupation Height are temperature-specific. Varying relationships between Larval and Pupal Developmental Time between and within populations also suggest stage-specific modifications of genetic architecture for this trait. This flexibility would allow for a somewhat independent evolution of adaptive traits at different environments and life stages, favoring the maintenance of genetic variability and thus sustaining the traits’ evolvabilities.     

Developmental structuring of phenotypic variation: A case study with a cellular automata model of ontogeny

Developmental mechanisms not only produce an organismal phenotype, but they also structure the way genetic variation maps to phenotypic variation. Here, we revisit a computational model for the evolution of ontogeny based on cellular automata, in which evolution regularly discovered two alternative mechanisms for achieving a selected phenotype, one showing high modularity, the other showing morphological integration. We measure a primary variational property of the systems, their distribution of fitness effects of mutation. We find that the modular ontogeny shows the evolution of mutational robustness and ontogenic simplification, while the integrated ontogeny does not. We discuss the wider use of this methodology on other computational models of development as well as real organisms.