Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution

Biologists have long sought to understand which genes and what kinds of changes in their sequences are responsible for the evolution of morphological diversity. Here, I outline eight principles derived from molecular and evolutionary developmental biology and review recent studies of species divergence that have led to a genetic theory of morphological evolution, which states that (1) form evolves largely by altering the expression of functionally conserved proteins, and (2) such changes largely occur through mutations in the cis-regulatory sequences of pleiotropic developmental regulatory loci and of the target genes within the vast networks they control.     

THE LOCI OF EVOLUTION: HOW PREDICTABLE IS GENETIC EVOLUTION?

Is genetic evolution predictable? Evolutionary developmental biologists have argued that, at least for morphological traits, the answer is a resounding yes. Most mutations causing morphological variation are expected to reside in the cis‐regulatory, rather than the coding, regions of developmental genes. This “cis‐regulatory hypothesis” has recently come under attack. In this review, we first describe and critique the arguments that have been proposed in support of the cis‐regulatory hypothesis. We then test the empirical support for the cis‐regulatory hypothesis with a comprehensive survey of mutations responsible for phenotypic evolution in multicellular organisms. Cis‐regulatory mutations currently represent approximately 22% of 331 identified genetic changes although the number of cis‐regulatory changes published annually is rapidly increasing. Above the species level, cis‐regulatory mutations altering morphology are more common than coding changes. Also, above the species level cis‐regulatory mutations predominate for genes not involved in terminal differentiation. These patterns imply that the simple question “Do coding or cis‐regulatory mutations cause more phenotypic evolution?” hides more interesting phenomena. Evolution in different kinds of populations and over different durations may result in selection of different kinds of mutations. Predicting the genetic basis of evolution requires a comprehensive synthesis of molecular developmental biology and population genetics.     

MicroRNA networks and developmental plasticity in plants

Plant microRNAs (miRNAs) are embedded in regulatory networks that coordinate different gene expression programs in support of developmental plasticity. Modification of miRNA-target nodes during evolution might in turn underlie morphological and physiological diversity. A survey of the literature indicates that miRNA-target nodes themselves are organized in networks, and here we discuss some of the developmental traits they control along with possible interactions between miRNA and their targets. Because miRNAs and their interactions are not only at the heart of regulating many aspects of developmental plasticity, but because they also have an inherently quantitative mode of action, they present important targets for biotechnology applications.     

Acoel development supports a simple planula-like urbilaterian

Molecular approaches to the study of development and evolution have had profound effects on our understanding of the nature of the evolutionary process. Developmental biologists became intoxicated with fanciful notions of reconstructing genetic pathways of morphogenesis while evolutionary biologists were sobered by the fallacy of reconstructing organismal relationships along increasing grades of morphological complexity. Increased taxon sampling and improvements in analytical techniques are providing a new approach and are forcing biologists to move past historical biases to allow more accurate mapping of morphological and developmental characters through evolutionary time. Here, we discuss the possible developmental and morphological features of the 'urbilaterian', the triploblastic animal with anterior-posterior and dorsoventral axes and predecessor of the protostome-deuterostome ancestor. We argue that this animal, with features resembling acoelomorph flatworms, was far simpler morphologically than the protostome-deuterostome ancestor despite possessing a nearly complete eubilaterian genome. We show that the deployment of some genes expected to pattern the protostome-deuterostome ancestor is not deployed in acoels in the predicted manner and thus might have been co-opted after the evolution of the urbilaterian. We also identify the developmental changes related to gastrulation that gave rise to the urbilaterian from a simpler cnidarian-like ancestor.     

A Reporter Assay in Lamprey Embryos Reveals Both Functional Conservation and Elaboration of Vertebrate Enhancers

The sea lamprey is an important model organism for investigating the evolutionary origins of vertebrates. As more vertebrate genome sequences are obtained, evolutionary developmental biologists are becoming increasingly able to identify putative gene regulatory elements across the breadth of the vertebrate taxa. The identification of these regions makes it possible to address how changes at the genomic level have led to changes in developmental gene regulatory networks and ultimately to the evolution of morphological diversity. Comparative genomics approaches using sea lamprey have already predicted a number of such regulatory elements in the lamprey genome. Functional characterisation of these sequences and other similar elements requires efficient reporter assays in lamprey. In this report, we describe the development of a transient transgenesis method for lamprey embryos. Focusing on conserved non-coding elements (CNEs), we use this method to investigate their functional conservation across the vertebrate subphylum. We find instances of both functional conservation and lineage-specific functional evolution of CNEs across vertebrates, emphasising the utility of functionally testing homologous CNEs in their host species.     

以发育模块重复征用和整合为基础的进化创新机制

进化新征的起源和分化是进化发育生物学研究的核心问题。通过对多细胞生物早期发育调控机制的比较分析,发现亲缘关系较远的生物所共有的一些形态特征受保守的发育调控程序调节（深同源性）。许多创新性状的发生是基于对预先存在的基因或发育调控模块的重复利用和整合。发育基因调控网络在结构和功能上高度模块化,因此不仅可以通过模块拆分和重复征用改变发育程式,而且也增强了调控网络自身的进化力。研究基因调控网络和发育系统的进化动态将有助于更深入地认识生物演化过程中创新性状发生和表型进化的分子机制。     

A spectrum of pleiotropic consequences in development due to changes in a regulatory pathway

Regulatory evolution has frequently been proposed as the primary mechanism driving morphological evolution. This is because regulatory changes may be less likely to cause deleterious pleiotropic effects than changes in protein structure, and consequently have a higher likelihood to be beneficial. We examined the potential for mutations in trans acting regulatory elements to drive phenotypic change, and the predictability of such change. We approach these questions by the study of the phenotypic scope and size of controlled alteration in the developmental network of the bacterium Myxococcus xanthus. We perturbed the expression of a key regulatory gene (fruA) by constructing independent in-frame deletions of four trans acting regulatory loci that modify its expression. While mutants retained developmental capability, the deletions caused changes in the expression of fruA and a dramatic shortening of time required for completion of development. We found phenotypic changes in the majority of traits measured, indicating pleiotropic effects of changes in regulation. The magnitude of the change for different traits was variable but the extent of differences between the mutants and parental type were consistent with changes in fruA expression. We conclude that changes in the expression of essential regulatory regions of developmental networks may simultaneously lead to modest as well as dramatic morphological changes upon which selection may subsequently act.     

Gene regulatory landscape of the sonic hedgehog locus in embryonic development

The organs of vertebrate species display a wide variety of morphology. A remaining challenge in evolutionary developmental biology is to elucidate how vertebrate lineages acquire distinct morphological features. Developmental programs are driven by spatiotemporal regulation of gene expression controlled by hundreds of thousands of cis-regulatory elements. Changes in the regulatory elements caused by the introduction of genetic variants can confer regulatory innovation that may underlie morphological novelties. Recent advances in sequencing technology have revealed a number of potential regulatory variants that can alter gene expression patterns. However, a limited number of studies demonstrate causal dependence between genetic and morphological changes. Regulation of Shh expression is a good model to understand how multiple regulatory elements organize tissue-specific gene expression patterns. This model also provides insights into how evolution of molecular traits, such as gene regulatory networks, lead to phenotypic novelty.     

The genetics and evo-devo of butterfly wing patterns

Understanding how the spectacular diversity of colour patterns on butterfly wings is shaped by natural selection, and how particular pattern elements are generated, has been the focus of both evolutionary and developmental biologists. The growing field of evolutionary developmental biology has now begun to provide a link between genetic variation and the phenotypes that are produced by developmental processes and that are sorted by natural selection. Butterfly wing patterns are set to become one of the few examples of morphological diversity to be studied successfully at many levels of biological organization, and thus to yield a more complete picture of adaptive morphological evolution.     

调控进化与形态多样性

揭示导致生物体形态和结构多样性产生的原因和机制, 是进化生物学研究的重要内容。进化发育生物学的研究表明, 许多复杂的形态结构及其多样性, 都是通过对古老调控网络的修饰或改造来完成的。也就是说, 生物体形态和结构的多样化并不是像以前认为的是由基因编码区的变化造成的, 而更多的是取决于基因的调控进化。作为控制基因表达的关键组分, 基因调控区的顺式调控元件通过与特定反式作用因子结合, 精细调控基因表达的时、空和量。因此, 调控元件的获得、丢失、修饰或者改变都能引起基因表达模式的变化, 是形态和结构多样性产生的主要原因。本文结合近年来国际上在基因的调控进化方面所取得的进展, 总结了真核生物中基因调控的方式和特点, 阐述了调控进化的基本式样, 揭示了调控进化在生物进化(特别是形态和结构多样化)中的作用。     

Convergent occurrence of the developmental hourglass in plant and animal embryogenesis?

Background The remarkable similarity of animal embryos at particular stages of development led to the proposal of a developmental hourglass. In this model, early events in development are less conserved across species but lead to a highly conserved ‘phylotypic period’. Beyond this stage, the model suggests that development once again becomes less conserved, leading to the diversity of forms. Recent comparative studies of gene expression in animal groups have provided strong support for the hourglass model. How and why might such an hourglass pattern be generated? More importantly, how might early acting events in development evolve while still maintaining a later conserved stage?Scope The discovery that an hourglass pattern may also exist in the embryogenesis of plants provides comparative data that may help us explain this phenomenon. Whether the developmental hourglass occurs in plants, and what this means for our understanding of embryogenesis in plants and animals is discussed. Models by which conserved early-acting genes might change their functional role in the evolution of gene networks, how networks buffer these changes, and how that might constrain, or confer diversity, of the body plan are also discused.Conclusions Evidence of a morphological and molecular hourglass in plant and animal embryogenesis suggests convergent evolution. This convergence is likely due to developmental constraints imposed upon embryogenesis by the need to produce a viable embryo with an established body plan, controlled by the architecture of the underlying gene regulatory networks. As the body plan is largely laid down during the middle phases of embryo development in plants and animals, then it is perhaps not surprising this stage represents the narrow waist of the hourglass where the gene regulatory networks are the oldest and most robust and integrated, limiting species diversity and constraining morphological space.     

French tradition and the rise of Evo-devo

The limited value most French biologists attributed to Darwinism and Mendelism in the first half of the twentieth century, and their conviction that these theories were at best insufficient to explain evolution and development, probably created conditions propitious to the development of Evo-devo at the end of the century. The separation between embryology and evolution did not exist in French biology as it did in American genetics: explanations for these two phenomena were sought equally in the “organization” of the egg. The major contribution of French biologists to Evo-devo was clearly the invention of the notion of the regulatory gene by Jacob and Monod; not the operon model per se, but the introduction of a hierarchy between two different kinds of genes. The consequence, the rise of the developmental gene concept, was not immediate, and required the active role of other biologists such as Antonio Garcia-Bellido, Allan Wilson and Stephen Jay Gould. Various obstacles had to be overcome for this concept of developmental gene to be fully accepted.     

Signals and regulators that govern Streptomyces development

Streptomyces coelicolor is the genetically best characterized species of a populous genus belonging to the gram-positive Actinobacteria. Streptomycetes are filamentous soil organisms, well known for the production of a plethora of biologically active secondary metabolic compounds. The Streptomyces developmental life cycle is uniquely complex and involves coordinated multicellular development with both physiological and morphological differentiation of several cell types, culminating in the production of secondary metabolites and dispersal of mature spores. This review presents a current appreciation of the signaling mechanisms used to orchestrate the decision to undergo morphological differentiation, and the regulators and regulatory networks that direct the intriguing development of multigenomic hyphae first to form specialized aerial hyphae and then to convert them into chains of dormant spores. This current view of S.?coelicolor development is destined for rapid evolution as data from '-omics' studies shed light on gene regulatory networks, new genetic screens identify hitherto unknown players, and the resolution of our insights into the underlying cell biological processes steadily improve.     

Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development

The tetrapod limb, which has served as a paradigm for the study of development and morphological evolution, is becoming a paradigm for developmental evolution as well. In its origin and diversification, the tetrapod limb has undergone a great deal of remodeling. These morphological changes and other evolutionary phenomena have produced variation in mechanisms of tetrapod limb development. Here, we review that variation in the four major clades of limbed tetrapods. Comparisons in a phylogenetic context reveal details of development and evolution that otherwise may have been unclear. Such details include apparent differences in the mechanisms of dorsal-ventral patterning and limb identity specification between mouse and chick and mechanistic novelties in amniotes, anurans, and urodeles. As we gain a better understanding of the details of limb development, further differences among taxa will be revealed. The use of appropriate comparative techniques in a phylogenetic context thus sheds light on evolutionary transitions in limb morphology and the generality of developmental models across species and is therefore important to both evolutionary and developmental biologists.     

Exploring alternative models of rostral-caudal patterning in the zebrafish neurectoderm with computer simulations

The StarLogo and NetLogo programming environments allow developmental biologists to build computer models of cell-cell interactions in an epithelium and visualize emergent properties of hypothetical genetic regulatory networks operating in the cells. These environments were used to explore alternative models that show how a posteriorizing morphogen gradient might define gene-expression domains along the rostral-caudal axis in the zebrafish neurectoderm. The models illustrate how a hypothetical genetic network based on auto-activation and cross-repression could lead to establishment of discrete non-overlapping gene-expression domains.     

Functional evolutionary developmental biology (evo‐devo) of morphological novelties in plants

Abstract The origin of morphological and ecological novelties is a long‐standing problem in evolutionary biology. Understanding these processes requires investigation from both the development and evolution standpoints, which promotes a new research field called “evolutionary developmental biology” (evo‐devo). The fundamental mechanism for the origin of a novel structure may involve heterotopy, heterochrony, ectopic expression, or loss of an existing regulatory factor. Accordingly, the morphological and ecological traits controlled by the regulatory genes may be gained, lost, or regained during evolution. Floral morphological novelties, for example, include homeotic alterations (related to organ identity), symmetric diversity, and changes in the size and morphology of the floral organs. These gains and losses can potentially arise through modification of the existing regulatory networks. Here, we review current knowledge concerning the origin of novel floral structures, such as “evolutionary homeotic mutated flowers”, floral symmetry in various plant species, and inflated calyx syndrome (ICS) within Solanaceae. Functional evo‐devo of the morphological novelties is a central theme of plant evolutionary biology. In addition, the discussion is extended to consider agronomic or domestication‐related traits, including the type, size, and morphology of fruits (berries), within Solanaceae.