Conserved versus innovative features in animal body organization

The origin of evolutionary novelties is a central topic in evolutionary developmental biology (evo-devo) studies. In any new feature, there is a conserved component that is either structural or related to the underlying genetic control, but it is not always obvious what is really new and what is conserved. Nevertheless, disentangling this blending of old and new features is basic to understanding mechanisms of evolutionary change. The origin of arthropod appendages illustrates the complexity in tracing the origin of evolutionary novelties. At the base of the lineage, the main body axis was already segmented and antero-posteriorly patterned, and the genetic tool kit required to form lateral outgrowths was already available. The novelty was possibly the developmental decision to "read" the available axial information and to exploit it for differentiating segmentally patterned and axially segmented appendages. Some important novelties bridge the gap between what have been traditionally distinguished as systemic and local changes. For example, the origin of the body cavities evolved by several animal groups may have been initiated by simple changes in cell-to-cell adhesive properties. Any possible change in an existing ontogenetic pathway has the potential to generate novelties.     

On the origins of morphological disparity and its diverse developmental bases

It has been repeatedly claimed that morphological novelties are an unresolved problem in evolutionary theory. Several definitions of novelty exist but most emphasize that novelties imply qualitative changes on the phenotype and not the quantitative gradual changes favored in the neo-Darwinian approach to evolutionary theory. This article discusses how the concept of novelty is used to describe aspects of morphological evolution that are not satisfactorily explained under the modern synthesis. In this article, it is suggested that there is a repertoire of morphological changes rather than two discrete qualitatively different types of morphological change. How these different types of morphological changes can be understood from the diversity of developmental mechanisms existing in animal development is explored. Specifically, it is proposed that animal morphology and its variation can be understood from the spatial patterns produced by a set of basic developmental mechanisms and their combination. Some specific examples of these kinds of morphologic changes are explained.     

Evolutionary mechanisms: Modularity,morphogenetic fields of gene expression,genetic regulation

Modern concepts heterochrony mechanisms, taking into account the data on modularity of ontogenetic and evolutionary processes, morphogenetic fields of gene expression are considered. In the context of evolutionary changes, features of genetic regulation of heterochronies, and also suppression of gene activity by epigenetic regulation are analyzed. Features of the origin of evolutionary novelties due to heterochronies, macromutations, and divergence of duplicated genes, which result in the formation of new genes and gene families, are discussed.     

Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development

The tetrapod limb, which has served as a paradigm for the study of development and morphological evolution, is becoming a paradigm for developmental evolution as well. In its origin and diversification, the tetrapod limb has undergone a great deal of remodeling. These morphological changes and other evolutionary phenomena have produced variation in mechanisms of tetrapod limb development. Here, we review that variation in the four major clades of limbed tetrapods. Comparisons in a phylogenetic context reveal details of development and evolution that otherwise may have been unclear. Such details include apparent differences in the mechanisms of dorsal-ventral patterning and limb identity specification between mouse and chick and mechanistic novelties in amniotes, anurans, and urodeles. As we gain a better understanding of the details of limb development, further differences among taxa will be revealed. The use of appropriate comparative techniques in a phylogenetic context thus sheds light on evolutionary transitions in limb morphology and the generality of developmental models across species and is therefore important to both evolutionary and developmental biologists.     

Rebuilding ships while at sea—Character individuality,homology, and evolutionary innovation

How novel traits originate in evolution is still one of the most perplexing questions in Evolutionary Biology. Building on a previous account of evolutionary innovation, I here propose that evolutionary novelties are those individualized characters that are not homologous to any characters in the ancestor. To clarify this definition, I here provide a detailed analysis of the concepts of “character individuality” and “homology” first, before addressing their role for our understanding of evolutionary innovation. I will argue (1) that functional as well as structural considerations are important for character individualization; and (2) that compositional (structural) and positional homology need to be clearly distinguished to properly describe the evolutionary transformations of hierarchically structured characters. My account will therefore integrate functional and structural perspectives and put forward a new multi-level view of character identity and transformation.     

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.     

Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties

Evolutionary novelties represent challenges to biologists, particularly those who would like to understand the developmental and genetic changes responsible for their appearance. Most modern aphids possess two apparent evolutionary novelties: cyclical parthenogenesis (a life cycle with both sexual and asexual phases) and viviparity (internal development and live birth of progeny) in their asexual phase. Here I discuss the evolution of these apparent novelties from a developmental standpoint. Although a full understanding of the evolution of cyclical parthenogenesis and viviparity in aphids can seem a daunting task, these complex transitions can at least be broken down into a handful of steps. I argue that these should include the following: a differentiation of two developmentally distinct oocytes; de novo synthesis of centrosomes and modification of meiosis during asexual oogenesis; a loss or bypass of any cell cycle arrest and changes in key developmental events during viviparous oogenesis; and a change in how mothers specify the sexual vs. asexual fates of their progeny. Grappling with the nature of such steps and the order in which they occurred ought to increase our understanding and reduce the apparent novelty of complex evolutionary transitions. J. Exp. Zool. (Mol. Dev. Evol.) 318B:448-459, 2012. ? 2012 Wiley Periodicals, Inc.     

EvoRegen in animals: Time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes

How do animals regenerate specialised tissues or their entire body after a traumatic injury, how has this ability evolved and what are the genetic and cellular components underpinning this remarkable feat? While some progress has been made in understanding mechanisms, relatively little is known about the evolution of regenerative ability. Which elements of regeneration are due to lineage specific evolutionary novelties or have deeply conserved roots within the Metazoa remains an open question. The renaissance in regeneration research, fuelled by the development of modern functional and comparative genomics, now enable us to gain a detailed understanding of both the mechanisms and evolutionary forces underpinning regeneration in diverse animal phyla. Here we review existing and emerging model systems, with the focus on invertebrates, for studying regeneration. We summarize findings across these taxa that tell us something about the evolution of adult stem cell types that fuel regeneration and the growing evidence that many highly regenerative animals harbor adult stem cells with a gene expression profile that overlaps with germline stem cells. We propose a framework in which regenerative ability broadly evolves through changes in the extent to which stem cells generated through embryogenesis are maintained into the adult life history.     

Turtles as hopeful monsters.

A recently published study on the development of the turtle shell highlights the important role that development plays in the origin of evolutionary novelties. The evolution of the highly derived adult anatomy of turtles is a prime example of a macroevolutionary event triggered by changes in early embryonic development. Early ontogenetic deviation may cause patterns of morphological change that are not compatible with scenarios of gradualistic, stepwise transformation.     

Origins and evolution of biological novelty

Understanding the origins and impacts of novel traits has been a perennial interest in many realms of ecology and evolutionary biology. Here, we build on previous evolutionary and philosophical treatments of this subject to encompass novelties across biological scales and eco-evolutionary perspectives. By defining novelties as new features at one biological scale that have emergent effects at other biological scales, we incorporate many forms of novelty that have previously been treated in isolation (such as novelty from genetic mutations, new developmental pathways, new morphological features, and new species). Our perspective is based on the fundamental idea that the emergence of a novelty, at any biological scale, depends on its environmental and genetic context. Through this lens, we outline a broad array of generative mechanisms underlying novelty and highlight how genomic tools are transforming our understanding of the origins of novelty. Lastly, we present several case studies to illustrate how novelties across biological scales and systems can be understood based on common mechanisms of change and their environmental and genetic contexts. Specifically, we highlight how gene duplication contributes to the evolution of new complex structures in visual systems; how genetic exchange in symbiosis alters functions of both host and symbiont, resulting in a novel organism; and how hybridisation between species can generate new species with new niches.     

Polyembryony in parasitic wasps: evolution of a novel mode of development

Major developmental innovations have been associated with adaptive radiations that have allowed particular groups of organisms to occupy empty ecospace. Well-known developmental novelties associated with the conquest of new habitats include the evolution of the tetrapode limb, allowing the radiation of vertebrates into a terrestrial habitat, and formation of insect wings that permitted their dispersal into the air. However, an understanding of the evolutionary forces and molecular mechanisms behind developmental novelties still remains tenuous. A little-studied adaptive radiation in insects from the developmental perspective is the evolution of parasitism. The parasitic lifestyle has allowed parasitic insects to occupy a novel ecological niche where they have evolved a plethora of life history strategies and modes of embryogenesis, developing on or within the body of the host. One of the most striking adaptations to development within the body of the host includes polyembryonic development, where certain wasps form clonally up to 2000 embryos from a single egg. Taking advantage of well-established insect phylogeny, techniques developed in a model insect, the fruit fly, and a wealth of knowledge in comparative insect embryology, we are starting to tease apart the evolutionary events that have led to this novel mode of development in insects.     

以发育模块重复征用和整合为基础的进化创新机制

进化新征的起源和分化是进化发育生物学研究的核心问题。通过对多细胞生物早期发育调控机制的比较分析,发现亲缘关系较远的生物所共有的一些形态特征受保守的发育调控程序调节（深同源性）。许多创新性状的发生是基于对预先存在的基因或发育调控模块的重复利用和整合。发育基因调控网络在结构和功能上高度模块化,因此不仅可以通过模块拆分和重复征用改变发育程式,而且也增强了调控网络自身的进化力。研究基因调控网络和发育系统的进化动态将有助于更深入地认识生物演化过程中创新性状发生和表型进化的分子机制。     

Selection-Driven Divergence After Gene Duplication in Arabidopsis thaliana

Gene duplications are one of the most important mechanisms for the origin of evolutionary novelties. Even though various models of the fate of duplicated genes have been established, current knowledge about the role of divergent selection after gene duplication is rather limited. In this study, we analyzed sequence divergence in response to neo- and subfunctionalization of segmentally duplicated genes in the genome of Arabidopsis thaliana. We compared the genomes of A. thaliana and the poplar Populus trichocarpa to identify orthologous pairs of genes and their corresponding inparalogs. Maximum-likelihood analyses of the nonsynonymous and synonymous substitution rate ratio [Formula: see text] of pairs of A. thaliana inparalogs were used to detect differences in the evolutionary rates of protein coding sequences. We analyzed 1,924 A. thaliana paralogous pairs and our results indicate that around 6.9% show divergent ω values between the lineages for a fraction of sites. We observe an enrichment of regulatory sequences, a reduced level of co-expression and an increased number of substitutions that can be attributed to positive selection based on an McDonald-Kreitman type of analysis. Taken together, these results show that selection after duplication contributes substantially to gene novelties and hence functional divergence in plants.     

Phenotypic Novelty in EvoDevo: The Distinction Between Continuous and Discontinuous Variation and Its Importance in Evolutionary Theory

The introduction of novel phenotypic structures is one of the most significant aspects of organismal evolution. Yet the concept of evolutionary novelty is used with drastically different connotations in various fields of research, and debate exists about whether novelties represent features that are distinct from standard forms of phenotypic variation. This article contrasts four separate uses for novelty in genetics, population genetics, morphology, and behavioral science, before establishing how novelties are used in evolutionary developmental biology (EvoDevo). In particular, it is detailed how an EvoDevo-specific research approach to novelty produces insight distinct from other fields, gives the concept explanatory power with predictive capacities, and brings new consequences to evolutionary theory. This includes the outlining of research strategies that draw attention to productive areas of inquiry, such as threshold dynamics in development. It is argued that an EvoDevo-based approach to novelty is inherently mechanistic, treats the phenotype as an agent with generative potential, and prompts a distinction between continuous and discontinuous variation in evolutionary theory.     

What can we learn about ecology and evolution from the fossil record?

The increased application of abundance data embedded within a more detailed and precise environmental context is enabling paleontologists to explore more rigorously the dynamics and underlying processes of ecological and evolutionary change in deep time. Several recent findings are of special theoretical interest. Community membership is commonly more stable and persistent than expected by chance, even in the face of the extreme environmental changes of the Ice Ages, and major evolutionary novelties commonly lie dormant for tens of millions of years before the ecological explosions of the clades that possess them. As we discuss here, questions such as these cannot be adequately addressed without the use of the fossil record.     

Limb,tooth, beak: Three modes of development and evolutionary innovation of form

The standard model of evolutionary change of form, deriving from Darwin’s theory via the Modern Synthesis, assumes a gradualistic reshaping of anatomical structures, with major changes only occurring by many cycles of natural selection for marginal adaptive advantage. This model, with its assertion that a single mechanism underlies both micro- and macroevolutionary change, contains an implicit notion of development which is only applicable in some cases. Here we compare the embryological processes that shape the vertebrate limb bud, the mammalian tooth and the avian beak. The implied notion of development in the standard evolutionary picture is met only in the case of the vertebrate limb, a single-primordium organ with morphostatic shaping, in which cells rearrange in response to signalling centres which are essentially unchanged by cell movement. In the case of the tooth, a single-primordium organ with morphodynamic shaping in which the strengths and relationships between signalling centres is influenced by the cell and tissue movements they induce, and the beak, in which the final form is influenced by the collision and rearrangement of multiple tissue primordia, abrupt appearance of qualitatively different forms (i.e. morphological novelties) can occur with small changes in system parameters induced by a genetic change, or by an environmental factor whose effects can be subsequently canalized genetically. Bringing developmental mechanisms and, specifically, the material properties of tissues as excitable media into the evolutionary picture, demonstrates that gradualistic change for incremental adaptive advantage is only one of the possible modes of morphological evolution.     

The evolutionary origin and diversification of feathers

Progress on the evolutionary origin and diversification of feathers has been hampered by conceptual problems and by the lack of plesiomorphic feather fossils. Recently, both of these limitations have been overcome by the proposal of the developmental theory of the origin of feathers, and the discovery of primitive feather fossils on nonavian theropod dinosaurs. The conceptual problems of previous theories of the origin of feathers are reviewed, and the alternative developmental theory is presented and discussed. The developmental theory proposes that feathers evolved through a series of evolutionary novelties in developmental mechanisms of the follicle and feather germ. The discovery of primitive and derived fossil feathers on a diversity of coelurosaurian theropod dinosaurs documents that feathers evolved and diversified in nonavian theropods before the origin of birds and before the origin of flight. The morphologies of these primitive feathers are congruent with the predictions of the developmental theory. Alternatives to the theropod origin of feathers are critique and rejected. Hypotheses for the initial function of feathers are reviewed. The aerodynamic theory of feather origins is falsified, but many other functions remain developmentally and phylogenetically plausible. Whatever their function, feathers evolved by selection for a follicle that would grow an emergent tubular appendage. Feathers are inherently tubular structures. The homology of feathers and scales is weakly supported. Feathers are composed of a suite of evolutionary novelties that evolved by the duplication, hierarchical organization, interaction, dissociation, and differentiation of morphological modules. The unique capacity for modular subdivision of the tubular feather follicle and germ has fostered the evolution of numerous innovations that characterize feathers. The evolution of feather keratin and the molecular basis of feather development are also discussed.     

Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

Two embryonic tissues-the neural crest and the cranial placodes-give rise to most evolutionary novelties of the vertebrate head. These two tissues develop similarly in several respects: they originate from ectoderm at the neural plate border, give rise to migratory cells and develop into multiple cell fates including sensory neurons. These similarities, and the joint appearance of both tissues in the vertebrate lineage, may point to a common evolutionary origin of neural crest and placodes from a specialized population of neural plate border cells. However, a review of the developmental mechanisms underlying the induction, specification, migration and cytodifferentiation of neural crest and placodes reveals fundamental differences between the tissues. Taken together with insights from recent studies in tunicates and amphioxus, this suggests that neural crest and placodes have an independent evolutionary origin and that they evolved from the neural and non-neural side of the neural plate border, respectively.     

Genome size reduction can trigger rapid phenotypic evolution in invasive plants

Background and Aims

The study of rapid evolution in invasive species has highlighted the fundamental role played by founder events, emergence of genetic novelties through recombination and rapid response to new selective pressures. However, whether rapid adaptation of introduced species can be driven by punctual changes in genome organization has received little attention. In plants, variation in genome size, i.e. variation in the amount of DNA per monoploid set of chromosomes through loss or gain of repeated DNA sequences, is known to influence a number of physiological, phenological and life-history features. The present study investigated whether change in genome size has contributed to the evolution of greater potential of vegetative growth in invasive populations of an introduced grass.

Methods

The study was based on the recent demonstration that invasive genotypes of reed canarygrass (Phalaris arundinacea) occurring in North America have emerged from recombination between introduced European strains. The genome sizes of more than 200 invasive and native genotypes were measured and their genome size was related to their phenotypic traits measured in a common glasshouse environment. Population genetics data were used to infer phylogeographical relationships between study populations, and the evolutionary history of genome size within the study species was inferred.

Key Results

Invasive genotypes had a smaller genome than European native genotypes from which they are derived. This smaller genome size had phenotypic effects that increased the species'' invasive potential, including a higher early growth rate, due to a negative relationship between genome size and rate of stem elongation. Based on inferred phylogeographical relationships of invasive and native populations, evolutionary models were consistent with a scenario of genome reduction by natural selection during the invasion process, rather than a scenario of stochastic change.

Conclusions

Punctual reduction in genome size could cause rapid changes in key phenotypic traits that enhance invasive ability. Although the generality of genome size variation leading to phenotypic evolution and the specific genomic mechanisms involved are not known, change in genome size may constitute an important but previously under-appreciated mechanism of rapid evolutionary change that may promote evolutionary novelties over short time scales.Key words: Biological invasion, evolutionary models, genome size, Phalaris arundinacea, quantile regression, relative growth rate, rapid evolution     

Approaches to Macroevolution: 1. General Concepts and Origin of Variation

Approaches to macroevolution require integration of its two fundamental components, i.e. the origin and the sorting of variation, in a hierarchical framework. Macroevolution occurs in multiple currencies that are only loosely correlated, notably taxonomic diversity, morphological disparity, and functional variety. The origin of variation within this conceptual framework is increasingly understood in developmental terms, with the semi-hierarchical structure of gene regulatory networks (GRNs, used here in a broad sense incorporating not just the genetic circuitry per se but the factors controlling the timing and location of gene expression and repression), the non-linear relation between magnitude of genetic change and the phenotypic results, the evolutionary potential of co-opting existing GRNs, and developmental responsiveness to nongenetic signals (i.e. epigenetics and plasticity), all requiring modification of standard microevolutionary models, and rendering difficult any simple definition of evolutionary novelty. The developmental factors underlying macroevolution create anisotropic probabilities—i.e., an uneven density distribution—of evolutionary change around any given phenotypic starting point, and the potential for coordinated changes among traits that can accommodate change via epigenetic mechanisms. From this standpoint, “punctuated equilibrium” and “phyletic gradualism” simply represent two cells in a matrix of evolutionary models of phenotypic change, and the origin of trends and evolutionary novelty are not simply functions of ecological opportunity. Over long timescales, contingency becomes especially important, and can be viewed in terms of macroevolutionary lags (the temporal separation between the origin of a trait or clade and subsequent diversification); such lags can arise by several mechanisms: as geological or phylogenetic artifacts, or when diversifications require synergistic interactions among traits, or between traits and external events. The temporal and spatial patterns of the origins of evolutionary novelties are a challenge to macroevolutionary theory; individual events can be described retrospectively, but a general model relating development, genetics, and ecology is needed. An accompanying paper (Jablonski in Evol Biol 2017) reviews diversity dynamics and the sorting of variation, with some general conclusions.