Developmental system drift and flexibility in evolutionary trajectories

SUMMARY The comparative analysis of homologous characters is a staple of evolutionary developmental biology and often involves extrapolating from experimental data in model organisms to infer developmental events in non-model organisms. In order to determine the general importance of data obtained in model organisms, it is critical to know how often and to what degree similar phenotypes expressed in different taxa are formed by divergent developmental processes. Both comparative studies of distantly related species and genetic analysis of closely related species indicate that many characters known to be homologous between taxa have diverged in their morphogenetic or gene regulatory underpinnings. This process, which we call "developmental system drift" (DSD), is apparently ubiquitous and has significant implications for the flexibility of developmental evolution of both conserved and evolving characters. Current data on the population genetics and molecular mechanisms of DSD illustrate how the details of developmental processes are constantly changing within evolutionary lineages, indicating that developmental systems may possess a great deal of plasticity in their responses to natural selection.     

Mouse models and the evolutionary developmental biology of the skull

Understanding development is relevant to understanding evolutionbecause developmental processes structure the expression ofphenotypic variation upon which natural selection acts. Advancesin developmental biology are fueling a new synthesis of developmentaland evolutionary biology, but it remains unclear how to usedevelopmental information that largely derives from a few modelorganisms to test hypotheses about the evolutionary developmentalbiology of taxa such as humans and other primates that havenot been or are not amenable to direct study through experimentaldevelopmental biology. In this article, we discuss how and whenmodel organisms like mice are useful for studying the evolutionarydevelopmental biology of even rather distantly related and morphologicallydifferent groups like primates. A productive approach is tofocus on processes that are likely to play key roles in producingevolutionarily significant phenotypic variation across a largephylogenetic range. We illustrate this approach by applyingthe analysis of craniofacial variation in mouse mutant modelsto primate and human evolution.     

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.     

Developing the genotype-to-phenotype relationship in evolutionary theory: A primer of developmental features

For decades, there have been repeated calls for more integration across evolutionary and developmental biology. However, critiques in the literature and recent funding initiatives suggest this integration remains incomplete. We suggest one way forward is to consider how we elaborate the most basic concept of development, the relationship between genotype and phenotype, in traditional models of evolutionary processes. For some questions, when more complex features of development are accounted for, predictions of evolutionary processes shift. We present a primer on concepts of development to clarify confusion in the literature and fuel new questions and approaches. The basic features of development involve expanding a base model of genotype-to-phenotype to include the genome, space, and time. A layer of complexity is added by incorporating developmental systems, including signal-response systems and networks of interactions. The developmental emergence of function, which captures developmental feedbacks and phenotypic performance, offers further model elaborations that explicitly link fitness with developmental systems. Finally, developmental features such as plasticity and developmental niche construction conceptualize the link between a developing phenotype and the external environment, allowing for a fuller inclusion of ecology in evolutionary models. Incorporating aspects of developmental complexity into evolutionary models also accommodates a more pluralistic focus on the causal importance of developmental systems, individual organisms, or agents in generating evolutionary patterns. Thus, by laying out existing concepts of development, and considering how they are used across different fields, we can gain clarity in existing debates around the extended evolutionary synthesis and pursue new directions in evolutionary developmental biology. Finally, we consider how nesting developmental features in traditional models of evolution can highlight areas of evolutionary biology that need more theoretical attention.     

The Hydra model - a model for what?

The introductory personal remarks refer to my motivations for choosing research projects, and for moving from physics to molecular biology and then to development, with Hydra as a model system. Historically, Trembley's discovery of Hydra regeneration in 1744 was the beginning of developmental biology as we understand it, with passionate debates about preformation versus de novo generation, mechanisms versus organisms. In fact, seemingly conflicting bottom-up and top-down concepts are both required in combination to understand development. In modern terms, this means analysing the molecules involved, as well as searching for physical principles underlying development within systems of molecules, cells and tissues. During the last decade, molecular biology has provided surprising and impressive evidence that the same types of molecules and molecular systems are involved in pattern formation in a wide range of organisms, including coelenterates like Hydra, and thus appear to have been "invented" early in evolution. Likewise, the features of certain systems, especially those of developmental regulation, are found in many different organisms. This includes the generation of spatial structures by the interplay of self-enhancing activation and "lateral" inhibitory effects of wider range, which is a main topic of my essay. Hydra regeneration is a particularly clear model for the formation of defined patterns within initially near-uniform tissues. In conclusion, this essay emphasizes the analysis of development in terms of physical laws, including the application of mathematics, and insists that Hydra was, and will continue to be, a rewarding model for understanding general features of embryogenesis and regeneration.     

进化发育生物学--发育、进化和遗传的再联合

发育生物学和进化生物学,以及遗传学历史上曾一度是彼此不分的统一体,后来由于各自研究重点的不同和相应研究手段的独立发展彼此分道扬镳了。如今,由于分子遗传学研究手段的革新使得基因序列测定成为分析发育机理、区分物种和评估种间亲缘关系的常规手段,三者又在基因水平上再度统一起来了,并形成一门被称为进化发育生物学（ｅｖｏｌｕｔｉｏｎａｒｙ ｄｅｖｅｌｏｐｍｅｎｔａｌ ｂｉｏｌｏｇｙ）的新学科。     

On Novelty,Heterochrony and Developmental Constraints in a Complex Morphological Theory of Recapitulation: The Genus <Emphasis Type="Italic">Trophon</Emphasis> as a Case Study

Darwin proposed natural selection as the main evolutionary mechanism in 1859. However, he did not think that this was the only process by which new species were generated. It was the so-called Modern Synthesis who established natural selection as the only mechanism responsible for evolution. Since then, the evolutionary process is explained by the pair mutation-adaptation: new species are generated by the appearance of new mutations, which in case of allowing new adaptations to the environment, they will be fixed and organisms will survive, therefore resulting in new species. An alternative view to the plasticity promoted by the adaptationist program is to think organisms as truly organized structures, having different levels of structural organization, which would mean that not every form is possible, but only those that correspond to a certain building plan. This would be reflected in the appearance of structural constraints, showing the limits imposed to the organism during its evolutionary development. In this work, I studied the ontogeny and development of three species of the genus Trophon by geometric morphometrics, in order to clarify important concepts in evolutionary developmental biology (Evo-Devo). Integrating theoretical and empirical investigations, I could propose a new conceptual framework for heterochrony in a context of a complex theory of recapitulation. Furthermore, I could detect a developmental constraint in Trophon, which provided an opportunity to reconstruct the concept of constraint and propose a synthesis between heterochrony and constraint that explained evolution as a process fueled by them, that is, as directive and driving force.     

Emerging model systems in evo-devo: horned beetles and the origins of diversity

Horned beetles and beetle horns are emerging as a model system suited to address fundamental questions in evolutionary developmental biology. Here we briefly review the biology of horned beetles and highlight the unusual opportunities they provide for evo-devo research. We then summarize recent advances in the development of new approaches and techniques that are now available to scientists interested in working with these organisms. We end by discussing ways to implement and combine these new approaches to explore new frontiers in evo-devo research previously unavailable to reseachers working outside traditional model organisms.     

Homology and the hierarchy of biological systems

Homology is the similarity between organisms due to common ancestry. Introduced by Richard Owen in 1843 in a paper entitled "Lectures on comparative anatomy and physiology of the invertebrate animals", the concept of homology predates Darwin's "Origin of Species" and has been very influential throughout the history of evolutionary biology. Although homology is the central concept of all comparative biology and provides a logical basis for it, the definition of the term and the criteria of its application remain controversial. Here, I will discuss homology in the context of the hierarchy of biological organization. I will provide insights gained from an exemplary case study in evolutionary developmental biology that indicates the uncoupling of homology at different levels of biological organization. I argue that continuity and hierarchy are separate but equally important issues of homology.     

Assessing the prospects for a return of organisms in evolutionary biology

An argument has been raised from various perspectives against the Modern Synthesis (MS) in the past two decades: it has forgotten organisms. Niche construction theorists (Odling-Smee et al. 2003), developmental biologists like West-Eberhard (2003) and Evo-Devo elaborated various views which concur on a rehabilitation of the explanatory role of organisms, formerly neglected by an evolutionary science mostly centered on genes. This paper aims at assessing such criticisms by unraveling the specific arguments they use and evaluating how empirical findings may support them. In the first section, I review the usual critiques about the way MS treats organisms and show that the organisms-concerned critique is multifaceted, and I use the controversy about units of selection in order to show that purely conceptual and empirical arguments have been mixed up when organisms were concerned. In the second section, I consider successively the challenges raised to evolutionary MS by structuralist biologists and then the developmentalist challenge mostly raised by Evo-Devo. I distinguish what is purely conceptual among those criticisms and what mostly relies on recent empirical findings about genome activation, inheritance, and epigenetics. The last section discusses another program in MS, namely "evolutionary transitions" research, as enquiry into the emergence of organisms.     

Clonal crayfish as biological model: a review on marbled crayfish

Since the mid-twentieth century, numerous vertebrates and invertebrates have been used as model organisms and become indispensable tools for exploring a broad range of biological and ecological processes. Crayfish seem to be adequate models which resulted in their involvement in research. In the two decades since its discovery, ongoing research has confirmed that the marbled crayfish (Procambarus virginalis Lyko, 2017) is an ideal taxon in this regard, especially due to its almost continuous asexual reproduction providing a source of genetically identical offspring. This review provides an overview of the occurrence, biology, ecology, ethology, and human exploitation of marbled crayfish with primary focus on its use as a laboratory model organism as well as potential risks to native biota in case of its introduction. Genetic uniformity, ease of culture, and a broad behaviour repertoire fosters the use of marbled crayfish in epigenetics and developmental biology, as well as physiological, ecotoxicological, and ethological research. Marbled crayfish could be further exploited for basic and applied fields of science such as evolutionary biology and clonal tumour evolution. However, due to its high invasive potential in freshwater environments security measures must be taken to prevent its escape into the wild.     

Mechanisms of germ cell specification across the metazoans: epigenesis and preformation

Germ cells play a unique role in gamete production, heredity and evolution. Therefore, to understand the mechanisms that specify germ cells is a central challenge in developmental and evolutionary biology. Data from model organisms show that germ cells can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis). Here we review existing data on 28 metazoan phyla, which indicate that although preformation is seen in most model organisms, it is actually the less prevalent mode of germ cell specification, and that epigenetic germ cell specification may be ancestral to the Metazoa.     

Organisms as natural purposes: the contemporary evolutionary perspective

Kant's conception of organisms as natural purposes raises a challenge to the adequacy of mechanistic explanation in biology. Certain features of organisms appear to be inexplicable by appeal to mechanical law alone. Some biological phenomena, it seems, can only be accounted for teleologically. Contemporary evolutionary biology has by and large ignored this challenge. It is widely held that Darwin's theory of natural selection gives us an adequate, wholly mechanical account of the nature of organisms. In contemporary biology, the category of the organism plays virtually no explanatory role. Contemporary evolutionary biology is a science of sub-organismal entities-replicators. I argue that recent advances in developmental biology demonstrate the inadequacy of sub-organismal mechanism. The category of the organism, construed as a 'natural purpose' should play an ineliminable role in explaining ontogenetic development and adaptive evolution. According to Kant the natural purposiveness of organisms cannot be demonstrated to be an objective principle in nature, nor can purposiveness figure in genuine explain. I attempt to argue, by appeal to recent work on self-organization, that the purposiveness of organisms is a natural phenomenon, and, by appeal to the apparatus of invariance explanation, that biological purposiveness provides genuine, ineliminable biological explanations.     

Identifying candidate genes affecting developmental time in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>: pervasive pleiotropy and gene-by-environment interaction

Background  

Understanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait.     

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.     

Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework

Developmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism's fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability – also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism's health and fitness. Finally, we apply life‐course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism's early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross‐talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity.     

The evolutionary pattern of early life history in water currents

Explanation of the characteristics of the early developmental stage of organisms is an important problem in evolutionary biology. In studies to date, evolutionary biologists have proposed some theories that successfully explain egg size variation. Mesoscale water movements may transport early life stage organisms in the aquatic biosphere. We propose a novel biological view to explain the duration of the retention period at the spawning ground and egg size variations in aquatic organisms with a planktonic stage at least during the early part of their life history. We develop a life history model of the early life stage of such aquatic organisms that takes into account their adaptations to water currents and biotic environmental gradients in the currents. We hypothesize that the distance from the spawning grounds to the nursery grounds and the biological richness of the currents affect the adaptive life history design of these aquatic organisms, including adaptive retention time at the spawning ground and egg size. Various studies of fish biology describe in passing phenomena that suggest the validity of our deductions, but explicit empirical attempts to evaluate our predictions in the field of evolutional biology are needed.     

The morphogenesis of evolutionary developmental biology

The early studies of evolutionary developmental biology (Evo-Devo) come from several sources. Tributaries flowing into Evo-Devo came from such disciplines as embryology, developmental genetics, evolutionary biology, ecology, paleontology, systematics, medical embryology and mathematical modeling. This essay will trace one of the major pathways, that from evolutionary embryology to Evo-Devo and it will show the interactions of this pathway with two other sources of Evo-Devo: ecological developmental biology and medical developmental biology. Together, these three fields are forming a more inclusive evolutionary developmental biology that is revitalizing and providing answers to old and important questions involving the formation of biodiversity on Earth. The phenotype of Evo-Devo is limited by internal constraints on what could be known given the methods and equipment of the time and it has been framed by external factors that include both academic and global politics.     

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.     

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.