The origin and evolution of appendages

Current awareness of gene expression patterns and developmental mechanisms involved in the outgrowth and patterning of animal appendages contributes to our understanding of the origin and evolution of these body parts. Nevertheless, this vision needs to be complemented by a new adequate comparative framework, in the context of a factorial notion of homology. It may even be profitable to categorize as appendages also gut diverticula, body ingrowths and 'virtual appendages' such as the eye spots on butterfly wings. Another unwarranted framework is the Cartesian co-ordinate system onto which the appendages are currently described and where it is supposed that one patterning system exists for each separate Cartesian axis. It may be justified, instead, to look for correspondences between the appendages and the main body axis of the same animal, as the latter might be the source of the growth and patterning mechanisms which gave rise to the former. This hypothesis of axis paramorphisms is contrasted with the current hypothesis of gene co-option. Recapitulationism is a common fault in current Evo-Devo perspectives concerning the origin of the appendages, in that the evolutionary origin of appendages is often expected to be the same as one of the key mechanisms involved in the ontogenetic inception of appendage formation. This unwarranted perspective is also evident in the current debate on the nature of the default arthropod appendage. Most likely, a default arthropod appendage never did exist, as the first appendages probably developed along the trunk of an animal already patterned extensively along the antero-posterior body axis.     

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.     

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。     

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.     

Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers

To examine the role of development in the origin of evolutionary novelties, we investigated the developmental mechanisms involved in the formation of a complex morphological novelty-branched feathers. We demonstrate that the anterior-posterior expression polarity of Sonic hedgehog (Shh) and Bone morphogenetic protein 2 (Bmp2) in the primordia of feathers, avian scales, and alligator scales is conserved and phylogenetically primitive to archosaurian integumentary appendages. In feather development, derived patterns of Shh-Bmp2 signaling are associated with the development of evolutionarily novel feather structures. Longitudinal Shh-Bmp2 expression domains in the marginal plate epithelium between barb ridges provide a prepattern of the barbs and rachis. Thus, control of Shh-Bmp2 signaling is a fundamental component of the mechanism determining feather form (i.e., plumulaceous vs. pennaceous structure). We show that Shh signaling is necessary for the formation and proper differentiation of a barb ridge and that it is mediated by Bmp signaling. BMP signaling is necessary and sufficient to negatively regulate Shh expression within forming feather germs and this epistatic relationship is conserved in scale morphogenesis. Ectopic SHH and BMP2 signaling leads to opposing effects on proliferation and differentiation within the feather germ, suggesting that the integrative signaling between Shh and Bmp2 is a means to regulate controlled growth and differentiation of forming skin appendages. We conclude that Shh and Bmp signaling is necessary for the formation of barb ridges in feathers and that Shh and Bmp2 signaling constitutes a functionally conserved developmental signaling module in archosaur epidermal appendage development. We propose a model in which branched feather form evolved by repeated, evolutionary re-utilization of a Shh-Bmp2 signaling module in new developmental contexts. Feather animation Quicktime movies can be viewed at http://fallon.anatomy.wisc.edu/feather.html.     

Limbs and tail as evolutionarily diverging duplicates of the main body axis

SUMMARY Contrasting hypotheses have been proposed to explain the pervasive parallels in the patterning of arthropod and vertebrate appendages. These hypotheses either call for a common ancestor already provided with patterned appendages or body outgrowths, or for the recruitment in limb patterning of single genes or genetic cassettes originally used for purposes other than axis patterning. I suggest instead that body appendages such as arthropod and vertebrate limbs and chordate tails are evolutionarily divergent duplicates (paramorphs) of the main body axis, that is, its duplicates, albeit devoid of endodermal component. Thus, vertebrate limbs and arthropod limbs are not historical homologs, but homoplastic features only transitively related to real historical homologs. Thus, the main body axis and the axis of the appendages have distinct but not independent evolutionary histories and may be involved in processes of homeotic co-option producing effects of morphological assimilation. For instance, chordate segmentation may have originated in the posterior appendage (tail) and subsequently extended to the trunk.     

Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty

Background  

The characterization of the molecular changes that underlie the origin and diversification of morphological novelties is a key challenge in evolutionary developmental biology. The evolution of such traits is thought to rely largely on co-option of a toolkit of conserved developmental genes that typically perform multiple functions. Mutations that affect both a universal developmental process and the formation of a novelty might shed light onto the genetics of traits not represented in model systems. Here we describe three pleiotropic mutations with large effects on a novel trait, butterfly eyespots, and on a conserved stage of embryogenesis, segment polarity.     

Finalism in Darwinian and Lamarckian Evolution: Lessons from Epigenetics and Developmental Biology

Finalist (teleological) implications have been described for both Darwinian and Lamarckian theories, even though finalism appears to be more commonly associated with Lamarckism. Biologists have focused on finding final causes to explain evolutionary novelties through, for example, applying the ??what for??? question to address experimental observations. Now epigenetics, together with developmental biology, may allow us to focus on the efficient causes leading to evolutionary change, asking the ??how??? question, considering environmental influences as inducers of genomic change. This is a whole under-studied dimension in evolutionary studies. In this paper, I discuss how epigenetics and developmental biology can help integrate two important ways in which the environment affects evolution: through inducing or through restricting the emergence of new phenotypes. I also discuss which aspects of both theories should be reconsidered in the face of current knowledge in epigenetics and where the emphasis of evolutionary experiments should be placed. Important goals of evolution related epigenetic studies should be: (i) to experimentally consider the separation among the origin of characters in a lineage and its further fixation, in order to address these processes in a proper dimension, (ii) to build the cause-effect relation between the factors inducing epigenetic changes and consequent changes in population parameters, and (iii) to consider that the arising of new characters is modulated by physiological and developmental constraints, and that this process is not related to a purpose or focused to solve an ecological, physiological or evolutionary challenge.     

Homology,limbs, and genitalia

SUMMARY Similarities in genetic control between the main body axis and its appendages have been generally explained in terms of genetic co-option. In particular, arthropod and vertebrate appendages have been explained to invoke a common ancestor already provided with patterned body outgrowths or independent recruitment in limb patterning of genes or genetic cassettes originally used for purposes other than axis patterning. An alternative explanation is that body appendages, including genitalia, are evolutionarily divergent duplicates (paramorphs) of the main body axis. However, are all metazoan limbs and genitalia homologous? The concept of body appendages as paramorphs of the main body axis eliminates the requirement for the last common ancestor of limb-bearing animals to have been provided with limbs. Moreover, the possibility for an animal to express complex organs ectopically demonstrates that positional and special homology may be ontogenetically and evolutionarily uncoupled. To assess the homology of animal genitalia, we need to take into account three different sets of mechanisms, all contributing to their positional and/or special homology and respectively involved (1) in the patterning of the main body axis, (2) in axis duplication, followed by limb patterning mechanisms diverging away from those still patterning the main body axis (axis paramorphism), and (3) in controlling the specification of sexual/genital features, which often, but not necessarily, come into play by modifying already developed and patterned body appendages. This analysis demonstrates that a combinatorial approach to homology helps disentangling phylogenetic and ontogenetic layers of homology.     

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.     

Gray anatomy: phylogenetic patterns of somatic gonad structures and reproductive strategies across the Bilateria

The last common ancestor of extant bilaterian animals is oftenreferred to as "Urbilateria". Comparative studies of developmentin a variety of laboratory animals, both traditional model systemsand newer "emerging" models, have resulted in many proposalsas to the morphological and developmental genetic characteristicsof Urbilateria. Most of these proposals are concerned with thedevelopment and emergence of external morphology, such as appendages,eyes, and ectodermal segmentation. Less attention has been paidto the evolutionary developmental biology of organogenesis.Arguably, one of the most important aspects of urbilaterianorganogenesis would have been gonadogenesis, since Urbilateriamust have successfully generated gametes and developed a strategyfor extrusion and fertilization, in order to be the ancestorof all living Bilateria. This article considers what is knownabout gonadogenesis and reproductive strategies in extant metazoans,and searches for phylogenetic patterns that suggest what sharedcharacteristics of these processes Urbilateria might have displayed.I conclude that the data presently available cannot suggesthomologies of the somatic components of metazoan gonads, andthat convergent evolution has resulted in many different morphological,and possibly molecular genetic, solutions to the various problemsposed by sexual reproduction.     

Segmentation: mono- or polyphyletic?

Understanding the evolutionary origins of segmented body plans in the metazoa has been a long-standing fascination for scientists. Competing hypotheses explaining the presence of distinct segmented taxa range from the suggestion that all segmentation in the metazoa is homologous to the proposal that segmentation arose independently many times, even within an individual clade or species. A major new source of information regarding the extent of homology vs. homoplasy of segmentation in recent years has been an examination of the extent to which molecular mechanisms underlying the segmentation process are conserved, the rationale being that a shared history will be apparent by the presence of common molecular components of a developmental program that give rise to a segmented body plan. There has been substantial progress recently in understanding the molecular mechanisms underlying the segmentation process in many groups, specifically within the three overtly segmented phyla: Annelida, Arthropoda and Chordata. This review will discuss what we currently know about the segmentation process in each group and how our understanding of the development of segmented structures in distinct taxa have influenced the hypotheses explaining the presence of a segmented body plan in the metazoa.     

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.     

The application of functional morphology to evolutionary studies

Studies of functional morphology contribute in several ways to the understanding of evolutionary patterns and processes. The former include the unravelling of dependencies of characters and the construction of biomechanically feasible transformation schemes. Among the latter are the identification of structural novelties that facilitate a cascade of diverse structural changes, and the Identification of mechanisms that enable the incorporation of evolutionary novelties into the integrated organism. The study of mechanisms that maintain the match between form and function during evolutionary (and developmental) changes is a new and important area for evolutionary biologists.     

Drosophila sex combs as a model of evolutionary innovations

The diversity of animal and plant forms is shaped by nested evolutionary innovations. Understanding the genetic and molecular changes responsible for these innovations is therefore one of the key goals of evolutionary biology. From the genetic point of view, the origin of novel traits implies the origin of new regulatory pathways to control their development. To understand how these new pathways are assembled in the course of evolution, we need model systems that combine relatively recent innovations with a powerful set of genetic and molecular tools. One such model is provided by the Drosophila sex comb—a male‐specific morphological structure that evolved in a relatively small lineage related to the model species D. melanogaster. Our extensive knowledge of sex comb development in D. melanogaster provides the basis for investigating the genetic changes responsible for sex comb origin and diversification. At the same time, sex combs can change on microevolutionary timescales and differ spectacularly among closely related species, providing opportunities for direct genetic analysis and for integrating developmental and population‐genetic approaches. Sex comb evolution is associated with the origin of novel interactions between Hox and sex determination genes. Activity of the sex determination pathway was brought under the control of the Hox code to become segment‐specific, while Hox gene expression became sexually dimorphic. At the same time, both Hox and sex determination genes were integrated into the intrasegmental spatial patterning network, and acquired new joint downstream targets. Phylogenetic analysis shows that similar sex comb morphologies evolved independently in different lineages. Convergent evolution at the phenotypic level reflects convergent changes in the expression of Hox and sex determination genes, involving both independent gains and losses of regulatory interactions. However, the downstream cell‐differentiation programs have diverged between species, and in some lineages, similar adult morphologies are produced by different morphogenetic mechanisms. These features make the sex comb an excellent model for examining not only the genetic changes responsible for its evolution, but also the cellular processes that translate DNA sequence changes into morphological diversity. The origin and diversification of sex combs provides insights into the roles of modularity, cooption, and regulatory changes in evolutionary innovations, and can serve as a model for understanding the origin of the more drastic novelties that define higher order taxa.     

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.     

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.     

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.     

Embryology of Manekia naranjoana (Piperaceae) and the origin of tetrasporic, 16-nucleate female gametophytes in Piperales

The vast majority of flowering plant seeds contain a triploid endosperm formed by fertilization of a monosporic, Polygonum-type female gametophyte. However, evolutionary transitions to six other genetic constructs of endosperm are widespread, and six of seven known patterns are found in the order Piperales. Within Piperaceae, Manekia has not been described, and we report its female gametophyte to be tetrasporic and 16-nucleate at maturity. Manekia ontogeny is generally characterized by early establishment of a bipolar or weakly bipolar body plan and a binucleate central cell at maturity (Drusa-type pattern); however, ca. 16% of early stages had distinctly tetrapolar organization, and ca. 21% of mature specimens had a tetranucleate central cell (Penaea-type pattern, not previously reported in Piperaceae). An evolutionary developmental analysis indicates heterochrony, heterotopy, novelties, and sequence deletions have each played roles in modulating variation within Piperales. Our data suggest the common ancestor of Piperaceae was tetrasporic and retained a plesiomorphic bipolar body plan, producing a "functionally bisporic" form of triploid endosperm derived from the lineal descendants of two megaspores and a sperm. Developmental modifications of this tetrasporic, bipolar ontogeny can account for the origin of all three other known "true" tetrasporic endosperm genetic constructs, formed from derivatives of all four megaspores and a sperm. These derived endosperms in turn have higher ploidy, higher potential heterozygosity, and reduced genetic conflicts.