Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Studies of threespine stickleback developmental evolution: progress and promise

A promising route for understanding the origin and diversification of organismal form is through studies at the intersection of evolution and development (evo-devo). While much has been learned over the last two decades concerning macroevolutionary patterns of developmental change, a fundamental gap in the evo-devo synthesis is the integration of mathematical population and quantitative genetics with studies of how genetic variation in natural populations affects developmental processes. This micro-evo-devo synthesis requires model organisms with which to ask empirical questions. Threespine stickleback fish (Gasterosteus aculeatus), long a model for studying behavior, ecology and evolution, is emerging as a prominent model micro-evo-devo system. Research on stickleback over the last decade has begun to address the genetic basis of morphological variation and sex determination, and much of this work has important implications for understanding the genetics of speciation. In this paper we review recent threespine stickleback micro-evo-devo results, and outline the resources that have been developed to make this synthesis possible. The prospects for stickleback research to speed the micro-(and macro-) evo-devo syntheses are great, and this workhorse model system is well situated to continue contributing to our understanding of the generation of diversity in organismal form for many more decades.     

Phylogeny,fossils, and model systems in the study of evolutionary developmental biology

The emerging field of evolutionary developmental biology (evo-devo) continues to operate largely under a single paradigm. In this paradigm developmental regulatory genes and processes are compared among a collection of "model organisms" selected primarily on the basis of their historical utility in the study of development. This approach has proven to be extremely informative, revealing an unexpected deep evolutionary conservation among developmental genes and genetic systems. Despite its success, concern has been expressed regarding its limitations. We discuss the "model organism" paradigm in evo-devo research. Based on our interpretation of its limitations, we propose a separate but complementary approach that is centered on "model groups." These groups are selected on the basis of their taxonomic affinity and their relevance to questions of interest to evo-devo biologists. We further discuss the Tetraodontiformes (Teleostei, Pisces) as an example of a "model group" for the evo-devo study of vertebrate skeletal elements.     

In search of evolutionary developmental mechanisms: the 30-year gap between 1944 and 1974

The approach I have elected in this retrospective of how I became a student of evo-devo is both biographical and historical, a case study along the lines of Waddington's The Evolution of an Evolutionist ('75), although in my case it is the Evolution of an Evo-devoist. What were the major events that brought me to developmental biology and from there to evo-devo? They were, of course, specific to my generation, to the state of knowledge at the time, and to my own particular circumstances. Although exposed to evolution and embryology as an undergraduate in the 1960s, my PhD and post-PhD research programme lay within developmental biology until the early 1970s. An important formative influence on my studies as an undergraduate was the work of Conrad Hal Waddington (1905-1975), whose writings made me aware of genetic assimilation and gave me an epigenetic approach to my developmental studies. The switch to evo-devo (and my discovery of the existence of the neural crest), I owe to an ASZ (now SICB) symposium held in 1973.     

基因及其顺式调控元件在动物表型进化中的作用

顺式调控假说是当前进化发育生物学中重要的理论之一, 该假说认为顺式调控元件的进化是调控外表性状进化的主要遗传机制。然而越来越多的实验结果表明, 仅靠顺式调控假说远不足以解释复杂的进化发育过程, 其他因素也会导致表型的进化, 如：与顺式调控元件相联基因的蛋白序列改变; 基因及染色体组复制; 蛋白结构域与顺式调控元件的灵活性等。文章回顾了近年来顺式调控元件以及与顺式调控元件相联基因的进化发育研究, 探讨了进化发育生物学研究的新方法与新思路。     

Empowering plant evo-devo: virus induced gene silencing validates new and emerging model systems

It is increasingly recognized that current established model systems are not sufficient to understand the evolution of biodiversity. The main limitation in developing additional model systems is the difficulty or inability to perform functional studies of target genes. Evolutionary developmental (evo-devo) biologists have adopted a transient transgenic technique, developed over the last decade for agricultural applications, which is allowing functional studies in the most disparate plant lineages. From monocots to dicots and from herbs to trees, virus-induced gene silencing (VIGS) has opened up a world of opportunities in plant evo-devo.     

Using evolutionary genomics,transcriptomics, and systems biology to reveal gene networks underlying fungal development

Fungal model species have contributed to many aspects of modern biology, from biochemistry and cell biology to molecular genetics. Nevertheless, only a few genes associated with morphological development in fungi have been functionally characterized in terms of their genetic or molecular interactions. Evolutionary developmental biology in fungi faces challenges from a lack of fossil records and unresolved species phylogeny, to homoplasy associated with simple morphology. Traditionally, reductive approaches use genetic screens to reveal phenotypes from a large number of mutants; the efficiency of these approaches relies on profound prior knowledge of the genetics and biology of the designated development trait—knowledge which is often not available for even well-studied fungal model species. Reductive approaches become less efficient for the study of developmental traits that are regulated quantitatively by more than one gene via networks. Recent advances in genome-wide analysis performed in representative multicellular fungal models and non-models have greatly improved upon the traditional reductive approaches in fungal evo-devo research by providing clues for focused knockout strategies. In particular, genome-wide gene expression data across developmental processes of interest in multiple species can expedite the advancement of integrative synthetic and systems biology strategies to reveal regulatory networks underlying fungal development.     

Evo-devo and the evolution of social behavior

The integration of evolutionary biology with developmental genetics into the hybrid field of 'evo-devo' resulted in major advances in understanding multicellular development and morphological evolution. Here we show how insights from evo-devo can be applied to study the evolution of social behavior. We develop this idea by reviewing studies that suggest that molecular pathways controlling feeding behavior and reproduction in solitary insects are part of a 'genetic toolkit' underlying the evolution of a particularly complex form of social behavior, division of labor among workers in honeybee colonies. The evo-devo approach, coupled with advances in genomics for non-model genetic organisms, including the recent sequencing of the honeybee genome, promises to advance our understanding of the evolution of social behavior.     

植物进化发育生物学的形成与研究进展

植物进化发育生物学是最近十几年来才兴起的一门学科, 它是进化发育生物学的主要分支之一。进化发育生物学的产生经历了进化生物学与胚胎学、遗传学和发育生物学的三次大的综合, 其历史可追溯到19世纪初冯.贝尔所创立的比较胚胎学。相关研究曾沉寂了近一个世纪, 直到20世纪80年代早期, 动物中homeobox基因被发现, 90年代初花发育的 ABC模型被提出, 加之对发育相关基因研究的不断深入, 才使基因型与表型联系了起来, 进而促进了进化发育生物学的飞速发展。目前进化发育生物学已成为21世纪生命科学领域的研究热点之一。本文详细阐述了进化发育生物学产生和发展的历程, 综述了最近十几年来植物进化发育生物学的主要研究进展。文中重点介绍了与植物发育密切相关的MADS-box基因在植物各大类群中的研究现状, 讨论了植物进化发育生物学领域的研究成果对花被演化、花对称性以及叶的进化等重要问题的启示。     

植物进化发育生物学的形成与研究进展

植物进化发育生物学是最近十几年来才兴起的一门学科,它是进化发育生物学的主要分支之一。进化发育生物学的产生经历了进化生物学与胚胎学、遗传学和发育生物学的三次大的综合,其历史可追溯到19世纪初冯.贝尔所创立的比较胚胎学。相关研究曾沉寂了近一个世纪,直到20世纪80年代早期,动物中homeobox基因被发现,90年代初花发育的ABC模型被提出,加之对发育相关基因研究的不断深入,才使基因型与表型联系了起来,进而促进了进化发育生物学的飞速发展。目前进化发育生物学已成为21世纪生命科学领域的研究热点之一。本文详细阐述了进化发育生物学产生和发展的历程,综述了最近十几年来植物进化发育生物学的主要研究进展。文中重点介绍了与植物发育密切相关的MADS-box基因在植物各大类群中的研究现状,讨论了植物进化发育生物学领域的研究成果对花被演化、花对称性以及叶的进化等重要问题的启示。     

Evo-devo and accounting for Darwin's endless forms

Evo-devo has led to dramatic advances in our understanding of how the processes of development can contribute to explaining patterns of evolutionary diversification that underlie the endless forms of animal life on the Earth. This is increasingly the case not only for the origins of evolutionary novelties that permit new functions and open up new adaptive zones, but also for the processes of evolutionary tinkering that occur within the subsequent radiations of related species. Evo-devo has time and again yielded spectacular examples of Darwin''s notions of common ancestry and of descent with modification. It has also shown that the evolution of endless forms is more about the evolution of the regulatory machinery of ancient genes than the origin and elaboration of new genes. Evolvability, especially with respect to the capacity of a developmental system to evolve and to generate the variation in form for natural selection to screen, has become a pivotal focus of evo-devo. As a consequence, a balancing of the concept of endless forms in morphospace with a greater awareness of the potential for developmental constraints and bias is becoming more general. The prospect of parallel horizons opening up for the evolution of behaviour is exciting; in particular, does Sean Carroll''s phrase referring to old genes learning new tricks in the evolution of endless forms apply equally as well to patterns of diversity and disparity in behavioural trait-space?     

Characterization,efficient transformation and regeneration of Chirita pumila (Gesneriaceae), a potential evo-devo model plant

An efficient transformation and regeneration system is essential for functional investigation of developmental genes and related elements in the field of evolutionary developmental biology (evo-devo). Chirita pumila D. Don belongs to the Gesneriaceae family, one of the most basal groups in Lamiales sensu lato, and possesses many tractable biological features including annual habit, small plant size, short generation time, abundant offspring and low chromosome number. In addition, C. pumila has cleistogamous flowers with potential cross-pollination, a special phenomenon first reported herein in Gesneriaceae. Parameters affecting shoot induction and genetic transformation have been evaluated, including plant growth regulators, temperature, antibiotic concentration, pre- and co-culture duration, Agrobacterium cell density and infection time. Polymerase chain reaction and β-Glucuronidase (GUS) activity assays of T0 and T1 plants show that the GUS gene has been introduced into the host with stable and universal expression. The applicability of the transformation system in gene function investigation is further confirmed by transforming a GsNST1B gene from Glycine soja. This transformation system provides a valuable platform for deep function analyses of related genes and elements for a wide range of evo-devo studies, especially in the field of floral evolution, which would develop its potential of being a model organism in Lamiales s. l.     

Neutrality and Robustness in Evo-Devo: Emergence of Lateral Inhibition

Embryonic development is defined by the hierarchical dynamical process that translates genetic information (genotype) into a spatial gene expression pattern (phenotype) providing the positional information for the correct unfolding of the organism. The nature and evolutionary implications of genotype–phenotype mapping still remain key topics in evolutionary developmental biology (evo-devo). We have explored here issues of neutrality, robustness, and diversity in evo-devo by means of a simple model of gene regulatory networks. The small size of the system allowed an exhaustive analysis of the entire fitness landscape and the extent of its neutrality. This analysis shows that evolution leads to a class of robust genetic networks with an expression pattern characteristic of lateral inhibition. This class is a repertoire of distinct implementations of this key developmental process, the diversity of which provides valuable clues about its underlying causal principles.     

Modern evolutional developmental biology: Mechanical and molecular genetic or phenotypic approaches?

Heightened interest in the evolutionary problems of developmental biology in the 1980s was due to the success of molecular genetics and disappointment in the synthetic theory of evolution, where the chapters of embryology and developmental biology seem to have been left out. Modern evo-devo, which turned out to be antipodean to the methodology of the synthetic theory of evolution, propagandized in the development of evolutionary problems only the mechanical and molecular genetic approach to the evolution of ontogenesis, based on cellular and intercellular interactions. The phonotypical approach to the evaluation of evolutionary occurrences in ontogenesis, which aids in the joining of the genetic and epigenetic levels of research, the theory of natural selection, the nomogenetic conception, and the problem of the wholeness of the organism in onto- and phylogenesis may be against this. The phenotypic approach to ontogenesis is methodologically the most perspective for evolutionary developmental biology.     

Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity

Evolutionary Developmental Biology aims for a mechanistic understanding of phenotypic diversity, and present knowledge is largely based on gene expression and interaction patterns from a small number of well-known model organisms. However, our understanding of biological diversification depends on our ability to pinpoint the causes of natural variation at a micro-evolutionary level, and therefore requires the isolation of genetic and developmental variation in a controlled genetic background. The colour patterns of Heliconius butterflies (Nymphalidae: Heliconiinae) provide a rich suite of naturally occurring variants with striking phenotypic diversity and multiple taxonomic levels of variation. Diversification in the genus is well known for its dramatic colour-pattern divergence between races or closely related species, and for Müllerian mimicry convergence between distantly related species, providing a unique system to study the development basis of colour-pattern evolution. A long history of genetic studies has showed that pattern variation is based on allelic combinations at a surprisingly small number of loci, and recent developmental evidence suggests that pattern development in Heliconius is different from the eyespot determination of other butterflies. Fine-scale genetic mapping studies have shown that a shared toolkit of genes is used to produce both convergent and divergent phenotypes. These exciting results and the development of new genomic resources make Heliconius a very promising evo-devo model for the study of adaptive change.     

The Developmental Basis of Variational Modularity: Insights from Quantitative Genetics,Morphometrics, and Developmental Biology

Groups of correlated characters (variational modules) often are considered to be the result of dissociated local developmental factors, i.e., of a modular genotype–phenotype map. But certain sets of pleiotropic factors can equally well induce modular phenotypic variation—no local developmental factors are necessary for a modular covariance structure. It is thus not possible to infer genetic or developmental modularity from standing variation alone. Yet, only for approximately linear genotype–phenotype maps is the induced covariance structure stable over changes of the phenotypic mean. For larger genetic and phenotypic variation, such as on a macroevolutionary level, developmental effects often are nonlinear and variational modularity remains stable only when it is realized by local dissociated developmental factors with no overlap of pleiotropic ranges. The evo-devo concept of modularity concurs only at this macroevolutionary level with the quantitative notion of variational modularity. Empirical evidence on the genetic and developmental architecture underlying phenotypic variation is inconclusive and partly subject to methodological problems. Many studies seem to indicate modularized phenotypic variation and local clusters of QTL effects, whereas other studies find support for several alternative models of modularity and report continuous distributions of QTL effects. This inconsistency partly results from the neglect of spatial relationships among the measured traits. Given the complex development of higher organisms, a combination of pleiotropic factors and more local developmental effects with a hierarchical, overlapping, and more or less continuous distribution appears most likely.     

Written in stone: fossils, genes and evo-devo

Fossils give evo-devo a past. They inform phylogenetic trees to show the direction of evolution of developmental features, and they can reveal ancient body plans. Fossils also provide the primary data that are used to date past events, including divergence times needed to estimate molecular clocks, which provide rates of developmental evolution. Fossils can set boundaries for hypotheses that are generated from living developmental systems, and for predictions of ancestral development and morphologies. Finally, although fossils rarely yield data on developmental processes directly, informative examples occur of extraordinary preservation of soft body parts, embryos and genomic information.