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.     

Libbie Henrietta Hyman (1888-1969): from developmental mechanics to the evolution of animal body plans

Libbie Hyman is the most influential comparative invertebrate zoologist of the 20th century in the English-speaking world. During the first part of her career Hyman conducted experimental research on the metabolic and developmental physiology of a host of invertebrates and vertebrate embryos. One important aim of these studies was to elucidate the hidden processes of morphogenesis. Some of the papers from this early phase of Hyman's career already contain the seeds for her subsequent occupation with comparative embryology and morphology to address questions about animal body plan evolution and metazoan phylogeny. Hyman's views on invertebrate evolution and phylogeny have become widely incorporated into textbooks, and until very recently Hyman's ideas have been equated with 'traditional' or 'classical' views on animal evolution. Hyman's enduring fame and significance for modern evo-devo is primarily based upon her magisterial six-volume series The Invertebrates, which is the most encompassing single-author synthesis of invertebrate structure and development of the 20th century. In The Invertebrates Hyman addressed numerous questions about the evolution of animal body plans and metazoan phylogeny that are nowadays core items on the research agenda of evo-devo. In addition, Hyman had a lasting influence on teaching with the publication of her widely used laboratory manuals for elementary zoology, and especially comparative vertebrate anatomy.     

Reversing opinions on Dollo's Law

Dollo's Law, the idea that the loss of complex features in evolution is irreversible, is a popular concept in evolutionary biology. Here we review how application of recent phylogenetic methods, genomics and evo-devo approaches is changing our view of Dollo's Law and its underlying mechanisms. Phylogenetic studies have recently demonstrated cases where seemingly complex features such as digits and wings have been reacquired. Meanwhile, large genomics databases and evo-devo studies are showing how the underlying developmental pathways and genetic architecture can be retained after the loss of a character. With dwindling evidence for the law-like nature of Dollo's Law, we anticipate a return to Dollo's original focus on irreversibility of all kinds of changes, not exclusively losses.     

Evolution of networks for body plan patterning; interplay of modularity, robustness and evolvability

A major goal of evolutionary developmental biology (evo-devo) is to understand how multicellular body plans of increasing complexity have evolved, and how the corresponding developmental programs are genetically encoded. It has been repeatedly argued that key to the evolution of increased body plan complexity is the modularity of the underlying developmental gene regulatory networks (GRNs). This modularity is considered essential for network robustness and evolvability. In our opinion, these ideas, appealing as they may sound, have not been sufficiently tested. Here we use computer simulations to study the evolution of GRNs' underlying body plan patterning. We select for body plan segmentation and differentiation, as these are considered to be major innovations in metazoan evolution. To allow modular networks to evolve, we independently select for segmentation and differentiation. We study both the occurrence and relation of robustness, evolvability and modularity of evolved networks. Interestingly, we observed two distinct evolutionary strategies to evolve a segmented, differentiated body plan. In the first strategy, first segments and then differentiation domains evolve (SF strategy). In the second scenario segments and domains evolve simultaneously (SS strategy). We demonstrate that under indirect selection for robustness the SF strategy becomes dominant. In addition, as a byproduct of this larger robustness, the SF strategy is also more evolvable. Finally, using a combined functional and architectural approach, we determine network modularity. We find that while SS networks generate segments and domains in an integrated manner, SF networks use largely independent modules to produce segments and domains. Surprisingly, we find that widely used, purely architectural methods for determining network modularity completely fail to establish this higher modularity of SF networks. Finally, we observe that, as a free side effect of evolving segmentation and differentiation in combination, we obtained in-silico developmental mechanisms resembling mechanisms used in vertebrate development.     

Evo-devo and the I.I. Schmalhausen concept of the evolution of ontogeny

Evo-devo is considered a special field of knowledge emphasizing the role of developmental processes and mechanisms in evolution and integrating the data of many disciplines studying various structural levels of biosphere organization. A mechanical approach to estimation of events is regarded as a specific feature of the evo-devo concept. In our opinion, the I.I. Schmalhausen concept of the evolution of ontogeny, opposing the reductionist approach of many contemporary evo-devo adherents, can be regarded as the fundamental basis of evo-devo.     

Mark Q. Martindale: shedding new light on developmental diversity

The Saint-Petersburg Society of Naturalists awarded the 2009 "Alexander Kowalevsky Medal" to Mark Q. Martindale, Professor of Organismal Biology at the University of Hawaii and Director of the Kewalo Marine Laboratory, Honolulu. This international award inaugurated first in 1910 was re-established only in 2001. In memory of Alexander Onufrievich Kowalevsky, it is awarded to outstanding zoologists and embryologists who have made great contributions to the field of embryology and developmental biology from an evolutionary perspective. Mark Q. Martindale has worked on a wide range of animals, mostly marine species, in contrast to many evo-devo researchers who often use a single "well-established" model organism. His work demonstrates how the insights gained by studying less "popular" animal taxa not only complement, but also significantly enrich our knowledge of the evolution of metazoan body plans and of the events that have led to the current animal diversity.     

Evolution of wing pigmentation in Drosophila: Diversity,physiological regulation,and cis-regulatory evolution

Fruit flies (Drosophila and its close relatives, or “drosophilids”) are a group that includes an important model organism, Drosophila melanogaster, and also very diverse species distributed worldwide. Many of these species have black or brown pigmentation patterns on their wings, and have been used as material for evo-devo research. Pigmentation patterns are thought to have evolved rapidly compared with body plans or body shapes; hence they are advantageous model systems for studying evolutionary gains of traits and parallel evolution. Various groups of drosophilids, including genus Idiomyia (Hawaiian Drosophila), have a variety of pigmentations, ranging from simple black pigmentations around crossveins to a single antero-distal spot and a more complex mottled pattern. Pigmentation patterns are sometimes obviously used for sexual displays; however, in some cases they may have other functions. The process of wing formation in Drosophila, the general mechanism of pigmentation formation, and the transport of substances necessary for pigmentation, including melanin precursors, through wing veins are summarized here. Lastly, the evolution of the expression of genes regulating pigmentation patterns, the role of cis-regulatory regions, and the conditions required for the evolutionary emergence of pigmentation patterns are discussed. Future prospects for research on the evolution of wing pigmentation pattern formation in drosophilids are presented, particularly from the point of view of how they compare with other studies of the evolution of new traits.     

The Evolution of Plant Body Plans--A Biomechanical Perspective

Defining ‘plants’ inclusively as ‘photosyntheticeukaryotes’, four basic body plans are identifiable amongplant lineages (unicellular, siphonous, colonial and multicellular).All of these body plans occur in most plant lineages, but onlythe multicellular body plan was carried onto land by the embryophytes.Extensive morphological and anatomical homoplasy is evidentamong species with different body plans. This is ascribed tothe facts that the acquisition of nutrients and radiant energyis affected by plant body size, shape and geometry, and that,with the exception of the unicellular body plan, each of theother body plans involves an ‘open and indeterminate’ontogeny capable of modifying body size, shape and geometryregardless of how organized growth is achieved. In terms ofunicellular species, the available data indicate that size-dependentvariations in surface area, metabolic constituents (e.g. photosyntheticpigments), and reproductive rates limit maximum body size innutrient poor habitats or those that change rapidly or unpredictably.This maximum size can be exceeded in more stable niches by eitherthe cooperation of conspecific cells sharing a common extracellularmatrix (i.e. the ‘colonial’ body plan) or by repeatedmitotic cellular division associated with sustained cytoplasmic(symplastic) continuity (i.e. multicellularity). The siphonousplant body plan may have been evolutionarily derived from aunicellular or multicellular ancestral life form. Each of theplant body plans is reviewed in terms of its biomechanical advantagesand disadvantages. Variants of the multicellular body plan,especially those of the Chlorophyta, Charophyta, and Embryophyta,are given special emphasis. Copyright 2000 Annals of BotanyCompany Algae, biomechanics, body plans, body size, embryophytes, evolution, multicellularity, plants     

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.     

The Hox Paradox: More complex(es) than imagined

An understanding of the origin of different body plans requires knowledge of how the genes and genetic pathways that control embryonic development have evolved. The Hox genes provide an appealing starting point for such studies because they play a well-understood causal role in the regionalization of the body plan of all bilaterally symmetric animals. Vertebrate evolution has been characterized by gene, and possibly genome, duplication events, which are believed to have provided raw genetic material for selection to act upon. It has recently been established that the Hox gene organization of ray-finned fishes, such as the zebrafish, differs dramatically from that of their lobe-finned relatives, a group that includes humans and all the other widely used vertebrate model systems. This unusual Hox gene organization of zebrafish is the result of a duplication event within the ray-finned fish lineage. Thus, teleosts, such as zebrafish, have more Hox genes arrayed over more clusters (or "complexes") than do tetrapod vertebrates. Here, I review our understanding of Hox cluster architecture in different vertebrates and consider the implications of gene duplication for Hox gene regulation and function and the evolution of different body plans.     

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.     

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.     

Aspergillus biofilms: clinical and industrial significance

The biofilm phenotype is an increasingly important concept in mycological research. Recently, there has been a developing interest in whether Aspergillus species are truly able to form biofilms or not. Industrial mycologists have long been aware of biofilms and their benefit in fermentation processes, whereas clinically their role is uncertain. This review provides an update on the impact that Aspergillus biofilms have medically and industrially, and will discuss biofilm development, and our current understanding of its molecular basis. The role of exopolymeric substance and how this substance relates to antimicrobial recalcitrance will also be discussed.     

Functional evo-devo

Functional factors such as optimal design and adaptive value have been the central concern of evolutionary biology since the advent of the New Synthesis. By contrast, evolutionary developmental biology (evo-devo) has concentrated primarily on structural factors such as the ways in which body parts can be built. These different emphases have stood in the way of an integrated understanding of the role of development in evolution. Here, we try to bridge this gap by outlining the relevance of functional factors in evo-devo. We use modularity and the view of development as a flexible evolutionary system to outline a unified perspective that includes both structural and functional aspects.     

Cell division orientation and planar cell polarity pathways

The orientation of cell division has a crucial role in early embryo body plan specification, axis determination and cell fate diversity generation, as well as in the morphogenesis of tissues and organs. In many instances, cell division orientation is regulated by the planar cell polarity (PCP) pathways: the Wnt/Frizzled non-canonical pathway or the Fat/Dachsous/Four-jointed pathway. Firstly, using asymmetric cell division in both Drosophila and C. elegans, we describe the central role of the Wnt/Frizzled pathway in the regulation of asymmetric cell division orientation, focusing on its cooperation with either the Src kinase pathway or the heterotrimeric G protein pathway. Secondly, we describe our present understanding of the mechanisms by which the planar cell polarity pathways drive tissue morphogenesis by regulating the orientation of symmetric cell division within a field of cells. Finally, we will discuss the important avenues that need to be explored in the future to better understand how planar cell polarity pathways control embryo body plan determination, cell fate specification or tissue morphogenesis by mitotic spindle orientation.     

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.     

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。     

Key outcomes from stakeholder workshops at a symposium to inform the development of an Australian national plan for rare diseases

ABSTRACT: BACKGROUND: Calls have been made for governments to adopt a cohesive approach to rare diseases through the development of national plans. At present, Australia does not have a national plan for rare diseases. To progress such a plan an inaugural Australian Rare Diseases Symposium was held in Western Australia in April 2011. This paper describes the key issues identified by symposium attendees for the development of a national plan, compares these to the content of EUROPLAN and national plans elsewhere and discusses how the outcomes might be integrated for national planning. METHODS: The symposium was comprised of a series of plenary sessions followed by workshops. The topics covered were; 1) Development of national plans for rare diseases; 2) Patient empowerment; 3) Patient care, support and management; 4) Research and translation; 5) Networks, partnerships and collaboration. All stakeholders within the rare diseases community were invited to participate, including: people affected by rare diseases such as patients, carers, and families; clinicians and allied health practitioners; social and disability services; researchers; patient support groups; industry (e.g. pharmaceutical, biotechnology and medical device companies); regulators and policy-makers. RESULTS: All of these stakeholder groups were represented at the symposium. Workshop participants indicated the need for a national plan, a national peak body, a standard definition of 'rare diseases', education campaigns, lobbying of government, research infrastructure, streamlined whole-of-lifetime service provision, case co-ordination, early diagnosis, support for health professionals and dedicated funding. CONCLUSIONS: These findings are consistent with frameworks and initiatives being undertaken internationally (such as EUROPLAN), and with national plans in other countries. This implies that the development of an Australian national plan could plausibly draw on frameworks for plan development that have been proposed for use in other jurisdictions. The translation of the symposium outcomes to government policy (i.e. a national plan) requires the consideration of several factors such as the under-representation of some stakeholder groups (e.g. clinicians) and the current lack of evidence required to translate some of the symposium outcomes to policy options. The acquisition of evidence provides a necessary first step in a comprehensive planning approach.     

The place of development in mathematical evolutionary theory

Development plays a critical role in structuring the joint offspring-parent phenotype distribution. It thus must be part of any truly general evolutionary theory. Historically, the offspring-parent distribution has often been treated in such a way as to bury the contribution of development, by distilling from it a single term, either heritability or additive genetic variance, and then working only with this term. I discuss two reasons why this approach is no longer satisfactory. First, the regression of expected offspring phenotype on parent phenotype can easily be nonlinear, and this nonlinearity can have a pronounced impact on the response to selection. Second, even when the offspring-parent regression is linear, it is nearly always a function of the environment, and the precise way that heritability covaries with the environment can have a substantial effect on adaptive evolution. Understanding these complexities of the offspring-parent distribution will require understanding of the developmental processes underlying the traits of interest. I briefly discuss how we can incorporate such complexity into formal evolutionary theory, and why it is likely to be important even for traits that are not traditionally the focus of evo-devo research. Finally, I briefly discuss a topic that is widely seen as being squarely in the domain of evo-devo: novelty. I argue that the same conceptual and mathematical framework that allows us to incorporate developmental complexity into simple models of trait evolution also yields insight into the evolution of novel traits.