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.     

The choice of model organisms in evo-devo

Study of the model organisms of developmental biology was crucial in establishing evo-devo as a new discipline. However, it has been claimed that this limited sample of organisms paints a biased picture of the role of development in evolution. Consequently, judicious choice of new model organisms is necessary to provide a more balanced picture. The challenge is to determine the best criteria for choosing new model organisms, given limited resources.     

Evo-devo: extending the evolutionary synthesis

Evolutionary developmental biology (evo-devo) explores the mechanistic relationships between the processes of individual development and phenotypic change during evolution. Although evo-devo is widely acknowledged to be revolutionizing our understanding of how the development of organisms has evolved, its substantial implications for the theoretical basis of evolution are often overlooked. This essay identifies major theoretical themes of current evo-devo research and highlights how its results take evolutionary theory beyond the boundaries of the Modern Synthesis.     

Are we doomed to repeat history? A model of the past using tiger beetles (Coleoptera: Cicindelidae) and conservation biology to anticipate the future

Studies of conservation biology involving tiger beetles have become increasingly common in the last 15 years. Governments and NGOs in several countries have considered tiger beetles in making policy decisions of national conservation efforts and have found tiger beetles useful organisms for arguing broad conservation issues. We trace the evolution of the relationship between tiger beetle studies and conservation biology and propose that this history may in itself provide a model for anticipating developments and improvements in the ability of conservation biology to find effective goals, gather appropriate data, and better communicate generalizations to non-scientific decision makers, the public, and other scientists. According to the General Continuum of Scientific Perspectives on Nature model, earliest biological studies begin with natural history and concentrate on observations in the field and specimen collecting, followed by observing and measuring in the field, manipulations in the field, observations and manipulations in the laboratory, and finally enter theoretical science including systems analysis and mathematical models. Using a balance of historical and analytical approaches, we tested the model using scientific studies of tiger beetles (Coleoptera: Cicindelidae) and the field of conservation biology. Conservation biology and tiger beetle studies follow the historical model, but the results for conservation biology also suggest a more complex model of simultaneous parallel developments. We use these results to anticipate ways to better meet goals in conservation biology, such as actively involving amateurs, avoiding exclusion of the public, and improving language and style in scientific communication. CXLV, Studies of Tiger Beetles     

Whole-mount in situ hybridization in the Rotifer <Emphasis Type="Italic">Brachionus plicatilis</Emphasis> representing a basal branch of lophotrochozoans

In order to broaden the comparative scope of evolutionary developmental biology and to refine our picture of animal macroevolution, it is necessary to establish new model organisms, especially from previously underrepresented groups, like the Lophotrochozoa. We have established the culture and protocols for molecular developmental biology in the rotifer species Brachionus plicatilis Müller (Rotifera, Monogononta). Rotifers are nonsegmented animals with enigmatic basal position within the lophotrochozoans and marked by several evolutionary novelties like the wheel organ (corona), the median eye, and the nonpaired posterior foot. The expression of Bp-Pax-6 is shown using whole-mount in situ hybridization. The inexpensive easy culture and experimental tractability of Brachionus as well as the range of interesting questions to which it holds the key make it a promising addition to the "zoo" of evo-devo model organisms.     

Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Dung beetles (subfamily Scarabaeinae) are popular model organisms in ecology and developmental biology, and for the last two decades they have experienced a systematics renaissance with the adoption of modern phylogenetic approaches. Within this period 16 key phylogenies and numerous additional studies with limited scope have been published, but higher-level relationships of this pivotal group of beetles remain contentious and current classifications contain many unnatural groupings. The present study provides a robust phylogenetic framework and a revised classification of dung beetles. We assembled the so far largest molecular dataset for dung beetles using sequences of 8 gene regions and 547 terminals including the outgroup taxa. This dataset was analyzed using Bayesian, maximum likelihood and parsimony approaches. In order to test the sensitivity of results to different analytical treatments, we evaluated alternative partitioning schemes based on secondary structure, domains and codon position. We assessed substitution models adequacy using Bayesian framework and used these results to exclude partitions where substitution models did not adequately depict the processes that generated the data. We show that exclusion of partitions that failed the model adequacy evaluation has a potential to improve phylogenetic inference, but efficient implementation of this approach on large datasets is problematic and awaits development of new computationally advanced software. In the class Insecta it is uncommon for the results of molecular phylogenetic analysis to lead to substantial changes in classification. However, the results presented here are congruent with recent morphological studies and support the largest change in dung beetle systematics for the last 50 years. Here we propose the revision of the concepts for the tribes Deltochilini (Canthonini), Dichotomiini and Coprini; additionally, we redefine the tribe Sisyphini. We provide and illustrate synapomorphies and diagnostic characters supporting the new concepts to facilitate diagnosability of the redefined tribes. As a result of the proposed changes a large number of genera previously assigned to these tribes are now left outside the redefined tribes and are treated as incertae sedis. The present study redefines dung beetles classification and gives new insight into their phylogeny. It has broad implications for the systematics as well as for various ecological and evolutionary analyses in dung beetles.     

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.     

Unburdening evo-devo: ancestral attractions, model organisms, and basal baloney

Although flourishing, I argue that evo-devo is not yet a mature scientific discipline. Its philosophical foundation exhibits an internal inconsistency that results from a metaphysical confusion. In modern evolutionary biology, species and other taxa are most commonly considered as individuals. I accept this thesis to be the best available foundation for modern evolutionary biology. However, evo-devo is characterized by a remarkable degree of typological thinking, which instead treats taxa as classes. This metaphysical incompatibility causes much distorted thinking. In this paper, I will discuss the logical implications of accepting the individuality thesis for evo-devo. First, I will illustrate the degree to which typological thinking pervades evo-devo. This ranges from the relatively innocent use of typologically tainted language to the more serious misuse of differences between taxa as evidence against homology and monophyly, and the logically flawed concept of partial homology. Second, I will illustrate how, in a context of typological thinking, evo-devo's harmless preoccupation with distant ancestors has become transformed into a pernicious problem afflicting the choice of model organisms. I will expose the logical flaws underlying the common assumption that model organisms can be expected to represent the clades they are a part of in an unambiguous way. I will expose the logical flaws underlying the general assumption that basal taxa are the best available stand-ins for ancestors and that they best represent the clade of which they are a part, while also allowing for optimal extrapolation of results.     

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 of non-bilaterian animals

The non-bilaterian animals comprise organisms in the phyla Porifera, Cnidaria, Ctenophora and Placozoa. These early-diverging phyla are pivotal to understanding the evolution of bilaterian animals. After the exponential increase in research in evolutionary development (evo-devo) in the last two decades, these organisms are again in the spotlight of evolutionary biology. In this work, I briefly review some aspects of the developmental biology of nonbilaterians that contribute to understanding the evolution of development and of the metazoans. The evolution of the developmental genetic toolkit, embryonic polarization, the origin of gastrulation and mesodermal cells, and the origin of neural cells are discussed. The possibility that germline and stem cell lineages have the same origin is also examined. Although a considerable number of non-bilaterian species are already being investigated, the use of species belonging to different branches of non-bilaterian lineages and functional experimentation with gene manipulation in the majority of the non-bilaterian lineages will be necessary for further progress in this field.     

Conservation and co-option in developmental programmes: the importance of homology relationships

One of the surprising insights gained from research in evolutionary developmental biology (evo-devo) is that increasing diversity in body plans and morphology in organisms across animal phyla are not reflected in similarly dramatic changes at the level of gene composition of their genomes. For instance, simplicity at the tissue level of organization often contrasts with a high degree of genetic complexity. Also intriguing is the observation that the coding regions of several genes of invertebrates show high sequence similarity to those in humans. This lack of change (conservation) indicates that evolutionary novelties may arise more frequently through combinatorial processes, such as changes in gene regulation and the recruitment of novel genes into existing regulatory gene networks (co-option), and less often through adaptive evolutionary processes in the coding portions of a gene. As a consequence, it is of great interest to examine whether the widespread conservation of the genetic machinery implies the same developmental function in a last common ancestor, or whether homologous genes acquired new developmental roles in structures of independent phylogenetic origin. To distinguish between these two possibilities one must refer to current concepts of phylogeny reconstruction and carefully investigate homology relationships. Particularly problematic in terms of homology decisions is the use of gene expression patterns of a given structure. In the future, research on more organisms other than the typical model systems will be required since these can provide insights that are not easily obtained from comparisons among only a few distantly related model species.     

The road to modularity

A network of interactions is called modular if it is subdivided into relatively autonomous, internally highly connected components. Modularity has emerged as a rallying point for research in developmental and evolutionary biology (and specifically evo-devo), as well as in molecular systems biology. Here we review the evidence for modularity and models about its origin. Although there is an emerging agreement that organisms have a modular organization, the main open problem is the question of whether modules arise through the action of natural selection or because of biased mutational mechanisms.     

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

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 cont...     

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。     

The marbled crayfish: a new model organism for research on development, epigenetics and evolutionary biology

Model organisms have contributed significantly to the understanding of basic biological phenomena. Suitable animal models are at hand for some research disciplines like genetics, development and cell biology but are still sought after for others like epigenetics. Research of the last years has revealed that the marbled crayfish (Marmorkrebs), which was discovered in the mid-1990s, meets researchers' demands for a vigorous, genetically identical and eurytopic laboratory model very well. Its most prominent advantages are production of high numbers of genetically identical offspring, stepwise alteration of the phenotype by moulting, complex morphology and behaviour and sequential generation of segments and limbs. This paper first reviews the discovery and research history of the marbled crayfish, its biology and culture and its special advantages. It then discusses, based on the published data, its suitability as a laboratory model for various research disciplines. The greatest potential of the marbled crayfish lies in epigenetics and environmental epigenomics and in stem cell research and regeneration. The marbled crayfish also appears to be suitable for the investigation of the role of stochastic developmental variation and epigenetic inheritance in evolution and to contribute to evo-devo and eco-devo. This unique crayfish is even of some value for applied biologists, for example as a toxicological test species.     

The role of ontogeny in wood diversity and evolution

Evolutionary developmental biology (evo-devo) explores the link between developmental patterning and phenotypic change through evolutionary time. In this review, we highlight the scientific advancements in understanding xylem evolution afforded by the evo-devo approach, opportunities for further engagement, and future research directions for the field. We review evidence that (1) heterochrony—the change in rate and timing of developmental events, (2) homeosis—the ontogenetic replacement of features, (3) heterometry—the change in quantity of a feature, (4) exaptation—the co-opting and repurposing of an ancestral feature, (5) the interplay between developmental and capacity constraints, and (6) novelty—the emergence of a novel feature, have all contributed to generating the diversity of woods. We present opportunities for future research engagement, which combine wood ontogeny within the context of robust phylogenetic hypotheses, and molecular biology.