Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

The origin and diversification of evolutionary novelties-lineage-specific traits of new adaptive value-is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development.     

DEVELOPMENTAL STABILITY, DISEASE AND MEDICINE

Developmental stability reflects the ability of a genotype to undergo stable development of a phenotype under given environmental conditions. Deviations from developmental stability arise from the disruptive effects of a wide range of environmental and genetic stresses, and such deviations are usually measured in terms of fluctuating asymmetry and phenodeviants. Fluctuating asymmetry is the most sensitive indicator of the ability to cope with stresses during ontogeny. There is considerable evidence that developmental stability, and especially fluctuating asymmetry, is a useful measure of phenotypic and genetic quality, because it covaries negatively with performance in multiple fitness domains in many species, including humans. It is proposed that developmental stability is an important marker of human health. Our goal is to initiate formally the integration of the sciences of evolutionary biology, developmental biology and medicine. We believe that this integrative framework provides a significant addition to the growing field of Darwinian medicine. The literature linking developmental stability and disease in humans is reviewed. Recent biological theoretical treatments pertaining to developmental stability are applied to a range of human health issues such as genetic diseases, ageing and survival, subfertility, abortion, child maltreatment by parents, cancer, infectious diseases, physiological and mental health, and physical attractiveness as a health certification.     

Brain evolution and development: adaptation,allometry and constraint

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.     

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。     

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。     

ADAPTIVE RADIATIONS,ECOLOGICAL SPECIALIZATION,AND THE EVOLUTIONARY INTEGRATION OF COMPLEX MORPHOLOGICAL STRUCTURES

The evolutionary integration of complex morphological structures is a macroevolutionary pattern in which morphogenetic components evolve in a coordinated fashion, which can result from the interplay among processes of developmental, genetic integration, and different types of selection. We tested hypotheses of ecological versus developmental factors underlying patterns of within‐species and evolutionary integration in the mandible of phyllostomid bats, during the most impressive ecological and morphological radiation among mammals. Shape variation of mandibular morphogenetic components was associated with diet, and the transition of integration patterns from developmental to within‐species to evolutionary was examined. Within‐species (as a proxy to genetic) integration in different lineages resembled developmental integration regardless of diet specialization, however, evolutionary integration patterns reflected selection in different mandibular components. For dietary specializations requiring extensive functional changes in mastication patterns or biting, such as frugivores and sanguivores, the evolutionary integration pattern was not associated with expected within‐species or developmental integration. On the other hand, specializations with lower mastication demands or without major functional reorganization (such as nectarivores and carnivores), presented evolutionary integration patterns similar to the expected developmental pattern. These results show that evolutionary integration patterns are largely a result of independent selection on specific components regardless of developmental modules.     

Genetic mapping of developmental instability: design, model and algorithm

Developmental instability or noise, defined as the phenotypic imprecision of an organism in the face of internal or external stochastic disturbances, has been thought to play an important role in shaping evolutionary processes and patterns. The genetic studies of developmental instability have been based on fluctuating asymmetry (FA) that measures random differences between the left and the right sides of bilateral traits. In this article, we frame an experimental design characterized by a spatial autocorrelation structure for determining the genetic control of developmental instability for those traits that cannot be bilaterally measured. This design allows the residual environmental variance of a quantitative trait to be dissolved into two components due to permanent and random environmental factors. The degree of developmental instability is quantified by the relative proportion of the random residual variance to the total residual variance. We formulate a mixture model to estimate and test the genetic effects of quantitative trait loci (QTL) on the developmental instability of the trait. The genetic parameters including the QTL position, the QTL effects, and spatial autocorrelations are estimated by implementing the EM algorithm within the mixture model framework. Simulation studies were performed to investigate the statistical behavior of the model. A live example for poplar trees was used to map the QTL that control root length growth and its developmental instability from cuttings in water culture.     

Origin of evolutionary novelty: examples from limbs

Classic hypotheses of vertebrate morphology are being informed by new data and new methods. Long nascent issues, such as the origin of tetrapod limbs, are being explored by paleontologists, molecular biologists, and functional anatomists. Progress in this arena will ultimately come down to knowing how macroevolutionary differences between taxa emerge from the genetic and phenotypic variation that arises within populations. The assembly of limbs over developmental and evolutionary time offers examples of the major processes at work in the origin of novelties. Recent comparative developmental analyses demonstrate that many of the mechanisms used to pattern limbs are ancient. One of the major consequences of this phenomenon is parallelism in the evolution of anatomical structures. Studies of both the fossil record and intrapopulational variation of extant populations reveal regularities in the origin of variation. These examples reveal processes acting at the level of populations that directly affect the patterns of diversity observed at higher taxonomic levels.     

Male-specific flight apparatus development in Acyrthosiphon pisum (Aphididae, Hemiptera, Insecta): comparison with female wing polyphenism

Wing polymorphisms observed in many Insecta are important topics in developmental biology and ecology; these polymorphisms are a consequence of trade-offs between flight and other abilities. The pea aphid, Acyrthosiphon pisum, possesses 2 types of wing polymorphisms: One is a genetic wing polymorphism occurring in males, and the other is an environmental wing polyphenism seen in viviparous females. Although genetic and environmental cues for the 2 wing polymorphisms have been studied, differences in their developmental regulation have not been elucidated. In particular, there is little knowledge regarding the developmental processes in male wing polymorphism. Therefore, in this study, the development of flight apparatuses and external morphologies was compared among 3 male wing morphs (winged, wingless, and intermediate). These male developmental processes were subsequently compared with those of female wing morphs. Developmental differences between the male and female polymorphisms were identified in flight muscle development and degeneration but not in wing bud development. Furthermore, the nymphal periods of wingless and intermediate males were significantly shorter than that of winged males, indicating the adaptive significance of male winglessness. Overall, this study indicates that the male and female wing polymorphisms are based on different regulatory systems for flight apparatus development, which are probably the result of different adaptations under different selection pressures.     

Conserved genetic pathways associated with microphthalmia,anophthalmia, and coloboma

The human eye is a complex organ whose development requires extraordinary coordination of developmental processes. The conservation of ocular developmental steps in vertebrates suggests possible common genetic mechanisms. Genetic diseases involving the eye represent a leading cause of blindness in children and adults. During the last decades, there has been an exponential increase in genetic studies of ocular disorders. In this review, we summarize current success in identification of genes responsible for microphthalmia, anophthalmia, and coloboma (MAC) phenotypes, which are associated with early defects in embryonic eye development. Studies in animal models for the orthologous genes identified overlapping phenotypes for most factors, confirming the conservation of their function in vertebrate development. These animal models allow for further investigation of the mechanisms of MAC, integration of various identified genes into common developmental pathways and finally, provide an avenue for the development and testing of therapeutic interventions. Birth Defects Research (Part C) 105:96–113, 2015. © 2015 Wiley Periodicals, Inc.     

Developmental processes regulate craniofacial variation in disease and evolution

Variation in development mediates phenotypic differences observed in evolution and disease. Although the mechanisms underlying phenotypic variation are still largely unknown, recent research suggests that variation in developmental processes may play a key role. Developmental processes mediate genotype–phenotype relationships and consequently play an important role regulating phenotypes. In this review, we provide an example of how shared and interacting developmental processes may explain convergence of phenotypes in spliceosomopathies and ribosomopathies. These data also suggest a shared pathway to disease treatment. We then discuss three major mechanisms that contribute to variation in developmental processes: genetic background (gene–gene interactions), gene–environment interactions, and developmental stochasticity. Finally, we comment on evolutionary alterations to developmental processes, and the evolution of disease buffering mechanisms.     

Using evolutionary genomics,transcriptomics, and systems biology to reveal gene networks underlying fungal development

Fungal model species have contributed to many aspects of modern biology, from biochemistry and cell biology to molecular genetics. Nevertheless, only a few genes associated with morphological development in fungi have been functionally characterized in terms of their genetic or molecular interactions. Evolutionary developmental biology in fungi faces challenges from a lack of fossil records and unresolved species phylogeny, to homoplasy associated with simple morphology. Traditionally, reductive approaches use genetic screens to reveal phenotypes from a large number of mutants; the efficiency of these approaches relies on profound prior knowledge of the genetics and biology of the designated development trait—knowledge which is often not available for even well-studied fungal model species. Reductive approaches become less efficient for the study of developmental traits that are regulated quantitatively by more than one gene via networks. Recent advances in genome-wide analysis performed in representative multicellular fungal models and non-models have greatly improved upon the traditional reductive approaches in fungal evo-devo research by providing clues for focused knockout strategies. In particular, genome-wide gene expression data across developmental processes of interest in multiple species can expedite the advancement of integrative synthetic and systems biology strategies to reveal regulatory networks underlying fungal development.     

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。     

Towards a comprehensive integration of morphological and genetic studies of floral development

Floral developmental genetics has exploded as a discipline. In addition to the rich genetic database for well-established models (Arabidopsis, Antirrhinum, Zea), numerous species have become the focus of floral genomic and genetic initiatives. Extensive documentation of the developmental morphology of Arabidopsis flowers has facilitated the linkage of genes and morphology. Complete developmental series also need to be assembled for emerging systems of molecular studies of floral genes. We address issues of homology assessment in floral structures, emphasize the need for assembling a complete floral developmental series for each species studied molecularly and genetically, stress the importance of a common set of terminology, and suggest a set of 'landmarks' to designate major events in floral development. We compare the floral developmental series of three species with different floral morphologies and propose a consensus of developmental stages to facilitate comparison of gene expression patterns. Taxa occupying key phylogenetic positions offer great potential for generating hypotheses about the regulation of floral development.     

Phylogeny,fossils, and model systems in the study of evolutionary developmental biology

The emerging field of evolutionary developmental biology (evo-devo) continues to operate largely under a single paradigm. In this paradigm developmental regulatory genes and processes are compared among a collection of "model organisms" selected primarily on the basis of their historical utility in the study of development. This approach has proven to be extremely informative, revealing an unexpected deep evolutionary conservation among developmental genes and genetic systems. Despite its success, concern has been expressed regarding its limitations. We discuss the "model organism" paradigm in evo-devo research. Based on our interpretation of its limitations, we propose a separate but complementary approach that is centered on "model groups." These groups are selected on the basis of their taxonomic affinity and their relevance to questions of interest to evo-devo biologists. We further discuss the Tetraodontiformes (Teleostei, Pisces) as an example of a "model group" for the evo-devo study of vertebrate skeletal elements.     

The Hsp90 capacitor, developmental remodeling, and evolution: the robustness of gene networks and the curious evolvability of metamorphosis

Genetic capacitors moderate expression of heritable variation and provide a novel mechanism for rapid evolution. The prototypic genetic capacitor, Hsp90, interfaces stress responses, developmental networks, trait thresholds and expression of wide-ranging morphological changes in Drosophila and other organisms. The Hsp90 capacitor hypothesis, that stress-sensitive storage and release of genetic variation through Hsp90 facilitates adaptive evolution in unpredictable environments, has been challenged by the belief that Hsp90-buffered variation is unconditionally deleterious. Here we review recent results supporting the Hsp90 capacitor hypothesis, highlighting the heritability, selectability, and potential evolvability of Hsp90-buffered traits. Despite a surprising bias toward morphological novelty and typically invariable quantitative traits, Hsp90-buffered changes are remarkably modular, and can be selected to high frequency independent of the expected negative side-effects or obvious correlated changes in other, unselected traits. Recent dissection of cryptic signal transduction variation involved in one Hsp90-buffered trait reveals potentially dozens of normally silent polymorphisms embedded in cell cycle, differentiation and growth control networks. Reduced function of Hsp90 substrates during environmental stress would destabilize robust developmental processes, relieve developmental constraints and plausibly enables genetic network remodeling by abundant cryptic alleles. We speculate that morphological transitions controlled by Hsp90 may fuel the incredible evolutionary lability of metazoan life-cycles.     

The role of developmental plasticity in evolutionary innovation

Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.