Evo-devo and the search for homology (“sameness”) in biological systems

Developmental biology and evolutionary studies have merged into evolutionary developmental biology (“evo-devo”). This synthesis already influenced and still continues to change the conceptual framework of structural biology. One of the cornerstones of structural biology is the concept of homology. But the search for homology (“sameness”) of biological structures depends on our favourite perspectives (axioms, paradigms). Five levels of homology (“sameness”) can be identified in the literature, although they overlap to some degree: (i) serial homology (homonomy) within modular organisms, (ii) historical homology (synapomorphy), which is taken as the only acceptable homology by many biologists, (iii) underlying homology (i.e., parallelism) in closely related taxa, (iv) deep evolutionary homology due to the “same” master genes in distantly related phyla, and (v) molecular homology exclusively at gene level. The following essay gives emphasis on the heuristic advantages of seemingly opposing perspectives in structural biology, with examples mainly from comparative plant morphology. The organization of the plant body in the majority of angiosperms led to the recognition of the classical root–shoot model. In some lineages bauplan rules were transcended during evolution and development. This resulted in morphological misfits such as the Podostemaceae, peculiar eudicots adapted to submerged river rocks. Their transformed “roots” and “shoots” fit only to a limited degree into the classical model which is based on either–or thinking. It has to be widened into a continuum model by taking over elements of fuzzy logic and fractal geometry to accommodate for lineages such as the Podostemaceae.     

ESTs library from embryonic stages reveals tubulin and reflectin diversity in Sepia officinalis (Mollusca — Cephalopoda)

New molecular resources regarding the so-called “non-standard models” in biology extend the present knowledge and are essential for molecular evolution and diversity studies (especially during the development) and evolutionary inferences about these zoological groups, or more practically for their fruitful management. Sepia officinalis, an economically important cephalopod species, is emerging as a new lophotrochozoan developmental model. We developed a large set of expressed sequence tags (ESTs) from embryonic stages of S. officinalis, yielding 19,780 non-redundant sequences (NRS). Around 75% of these sequences have no homologs in existing available databases. This set is the first developmental ESTs library in cephalopods. By exploring these NRS for tubulin, a generic protein family, and reflectin, a cephalopod specific protein family,we point out for both families a striking molecular diversity in S. officinalis.     

Molecular biology of embryonic development: How far have we come in the last ten years?

The successes of molecular developmental biology over the last ten years have been particularly impressive in those directions favored by its major paradigms. New technologies have both guided and been guided by the progress of the field. I review briefly some of the major insights into embryonic development that have derived from research in four specific areas: early embryogenesis of various forms; “pattern formation”; evolutionary conservation of regulatory elements; and spatial mechanisms of gene regulation. There remain many major problem areas, some of which may require new orientations to solve.     

Lessons from EEO: Toward a Universal Evolutionary Curriculum

We propose a human-centered evolutionary curriculum based around the three questions: Who am I? Where do I come from? How do I fit in? We base our curriculum on our experiences as an evolutionary biologist/paleontologist (NE) and as a secondary level special education science teacher (GE)—and not least from our joint experience as co-editors-in-chief of this journal. Our proposed curriculum starts and ends with human biology and evolution, linking these themes with topics as diverse as the “tree of life” (systematics), anthropology, Charles Darwin, cultural evolution, ecology, developmental biology, molecular evolution/genetics, paleontology, and plate tectonics. The curriculum is “universal” as it is designed to be taught at all levels, K–16. The curriculum is flexible: “modules” may be expanded and contracted, reordered, or modified to fit specific grade level needs—and the requirements and interests of local curricula and teachers. We further propose that students utilize workbooks from online or printed sources to investigate the local answers to the general questions (e.g., “Who am I?”), while classroom instruction is focused on the larger scale issues outlined in the modules of our curriculum.     

Correlation of ontogenetic and evolutionary processes in view of achievements of modern genetics: Role of gene duplication

I.I. Schmalhausen’s concept about the interrelation of individual and historical development is analyzed from the positions of modern developmental biology and molecular genetics. The role of gene duplication in evolutionary, ontogenetic, and adaptable processes is discussed. The data on mechanisms of functional diversification of duplicated genes (exon-intron structural changes and point mutations) in these processes are submitted. The modern synthesis outlook in developmental biology is regarded.     

Quelques apports à la théorie de l’Évolution,de la « Synthèse orthodoxe » à la « Super synthèse évo-dévo » 1970–2009 : un point de vue

Some contributions to evolutionary theory, from the “orthodox” Synthesis to the “Evo-devo Super synthesis” 1970–2009: A point of view. The “Modern Synthesis” of evolutionary biology coalesced and revitalized evolutionary theory beginning in the 1930s. It stressed the explanatory power of natural selection and gradual change to account for the processes that govern natural populations today, as well as patterns in the history of life. In the past 40 years, the synthesis has been challenged on various fronts ranging from paleontology to developmental biology, systematics, biogeography, and molecular and developmental biology. Several of its central propositions have been modified and expanded as a result. How well the synthesis continues to be effective will depend on its continued ability to test its central propositions and the efficacy of its central mechanisms, particularly on the basis of new evidence from emerging fields of study.     

花、基因、禾本科

进化发育生物学的一个重要任务就是揭示形态多样性的分子基础,该领域的研究包含形态、形态发育相关基因和形态所属类群等三个要素。花/花序是进化发育生物学研究的首要对象,系统发育重建和个体发育剖析的结合将促进认知花的形态进化。发育相关基因的进化表现为等位基因遗传或表观遗传的突变,基因家族生与死的进化,不同基因组拥有独特的基因。运用形态学或序列分析方法很大程度揭示了禾本科植物花进化过程中的基因进化。试从学科问题、思路方法以及具体例子介绍植物进化发育生物学。     

The effect of development on the direction of evolution: toward a twenty-first century consensus

Summary One of the most important questions in evolutionary biology is: what orients the evolutionary process? That is, what causes evolution to proceed toward certain developmental trajectories, and hence phenotypes, rather than others? In particular, there has been prolonged controversy over whether the direction of evolution is determined solely by external factors or whether the nature of the ontogenetic process, and the ways in which it can be altered by mutations in developmental genes, may also play a major role. Here, I examine this issue, concentrating on the following: the possible evolutionary orienting role of “developmental bias;” the question of whether selection can and/or will break bias; the extent to which bias is already incorporated in quantitative genetic studies; and ways of approaching the possible role of bias in the origin of evolutionary novelties. Finally, I suggest that developmental bias may provide a focal point for the coming together of conceptual and practical approaches to evo‐devo.     

花、基因、禾本科

进化发育生物学的一个重要任务就是揭示形态多样性的分子基础, 该领域的研究包含形态、形态发育相关基因和形态所属类群等三个要素。花/花序是进化发育生物学研究的首要对象, 系统发育重建和个体发育剖析的结合将促进认知花的形态进化。发育相关基因的进化表现为等位基因遗传或表观遗传的突变, 基因家族生与死的进化, 不同基因组拥有独特的基因。运用形态学或序列分析方法很大程度揭示了禾本科植物花进化过程中的基因进化。试从学科问题、思路方法以及具体例子介绍植物进化发育生物学。     

Evolutionary developmental biology its roots and characteristics

The rise of evolutionary developmental biology was not the progressive isolation and characterization of developmental genes and gene networks. Many obstacles had to be overcome: the idea that all genes were more or less involved in development; the evidence that developmental processes in insects had nothing in common with those of vertebrates.Different lines of research converged toward the creation of evolutionary developmental biology, giving this field of research its present heterogeneity. This does not prevent all those working in the field from sharing the conviction that a precise characterization of evolutionary variations is required to fully understand the evolutionary process.Some evolutionary developmental biologists directly challenge the Modern Synthesis. I propose some ways to reconcile these apparently opposed visions of evolution. The turbulence seen in evolutionary developmental biology reflects the present entry of history into biology.     

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).     

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.     

Conflict theory of genomic imprinting in mammals

In mammals, some embryonic genes are expressed differently depending on whether they are inherited from the sperm or egg, a phenomenon known as genomic imprinting. The information on the parental origin is transmitted by an epigenetic mark. Both the molecular mechanisms and evolutionary processes of genomic imprinting have been studied extensively. Here, I illustrate the simplest evolutionary dynamics of imprinting evolution based on the “conflict theory,” by considering the evolution of a gene encoding an embryonic growth factor controlling the maternal resource supply. It demonstrates that (a) the autosomal genes controlling placenta development to modify maternal resource acquisition may evolve a strong asymmetry of gene expression, provided the mother has some chance of accepting multiple males. (b) The genomic imprinting may not evolve if there is a small fraction of recessive deleterious mutations on the gene. (c) The growth-enhancing genes should evolve to paternally expressed, while the growth-suppressing genes should evolve to maternally expressed. (d) The X-linked genes also evolve genomic imprinting, but the main evolutionary force is the sex difference in the optimal embryonic size. I discuss other aberrations that can be explained by the modified versions of the basic model.     

Deconstructing the long-standing a priori assumption that serial homology generally involves ancestral similarity followed by anatomical divergence

It has long been assumed that serial homologues are ancestrally similar—polysomerism resulting from a “duplication” or “repetition” of forms—and then often diverge—anisomerism, for example, as they become adapted to perform different tasks as is the case with the forelimb and hind limbs of humans. However, such an assumption, with crucial implications for comparative, evolutionary, and developmental biology, and for evolutionary developmental biology, has in general not really been tested by a broad analysis of the available empirical data. Perhaps not surprisingly, more recent anatomical comparisons, as well as molecular knowledge of how, for example, serial appendicular structures are patterned along with different anteroposterior regions of the body axis of bilateral animals, and how “homologous” patterning domains do not necessarily mark “homologous” morphological domains, are putting in question this paradigm. In fact, apart from showing that many so-called “serial homologues” might not be similar at all, recent works have shown that in at least some cases some “serial” structures are indeed more similar to each other in derived taxa than in phylogenetically more ancestral ones, as pointed out by authors such as Owen. In this article, we are taking a step back to question whether such assumptions are actually correct at all, in the first place. In particular, we review other cases of so-called “serial homologues” such as insect wings, arthropod walking appendages, Dipteran thoracic bristles, and the vertebrae, ribs, teeth, myomeres, feathers, and hairs of chordate animals. We show that: (a) there are almost never cases of true ancestral similarity; (b) in evolution, such structures—for example, vertebra—and/or their subparts—for example, “transverse processes”—many times display trends toward less similarity while in many others display trends toward more similarity, that is, one cannot say that there is a clear, overall trend to anisomerism.     

The evolution of developmental mechanisms

Over the past two to three decades, developmental biology has demonstrated that all multicellular organisms in the animal kingdom share many of the same molecular building blocks and many of the same regulatory genetic pathways. Yet we still do not understand how the various organisms use these molecules and pathways to assume all the forms we know today. Evolutionary developmental biology tackles this problem by comparing the development of one organism to another and comparing the genes involved and gene functions to understand what makes one organism different from another. In this review, we revisit a set of seven concepts defined by Lewis Wolpert (fate maps, asymmetric division, induction, competence, positional information, determination, and lateral inhibition) that describe the characters of many developmental systems and supplement them with three additional concepts (developmental genomics, genetic redundancy, and genetic networks). We will discuss examples of comparative developmental studies where these concepts have guided observations on the advent of a developmental novelty. Finally, we identify a set of evolutionary frameworks, such as developmental constraints, cooption, duplication, parallel and convergent evolution, and homoplasy, to adequately describe the evolutionary properties of developmental systems.     

Russian comparative embryology takes form: a conceptual metamorphosis toward “evo‐devo”

This essay recapitulates major paths followed by the Russian tradition of what we refer to today as evolutionary developmental biology (“evo‐devo”). The article addresses several questions regarding the conceptual history of evolutionary embryological thought in its particularly Russian perspective: (1) the assertion by the St. Petersburg academician Wolff regarding the possible connections between environmental modifications during morphogenesis and the “transformation” of species, (2) the discovery of shared “principles” underlying animal development by von Baer, (3) the experimental expression of Baer's principles by Kowalevsky and Mechnikoff, (4) Severtsov's theory of phylembryogenesis, (5) Filatov's approach to the study of evolution using comparative “developmental mechanics”, and (6) Shmalgausen's concept of “stabilizing” selection as an attempt to elucidate the evolution of developmental mechanisms. The focus on comparative evolutionary embryology, which was established by Kowalevsky and Mechnikoff, still continues to be popular in present‐day “evo‐devo” research in Russia.     

The proximate/ultimate distinction in the multiple careers of Ernst Mayr

Ernst Mayr's distinction between “ultimate” and “proximate” causes is justly considered a major contribution to philosophy of biology. But how did Mayr come to this “philosophical” distinction, and what role did it play in his earlier “scientific” work? I address these issues by dividing Mayr's work into three careers or phases: 1) Mayr the naturalist/researcher, 2) Mayr the representative of and spokesman for evolutionary biology and systematics, and more recently 3) Mayr the historian and philosopher of biology. If we want to understand the role of the proximate/ultimate distinction in Mayr's more recent career as a philosopher and historian, then it helps to consider hisearlier use of the distinction, in the course of his research, and in his promotion of the professions of evolutionary biology and systematics. I believe that this approach would also shed light on some other important “philosophical” positions that Mayr has defended, including the distinction between “essentialism: and “population thinking.”