Robustness seems to be the opposite of evolvability. If phenotypes are robust against mutation, we might expect that a population will have difficulty adapting to an environmental change, as several studies have suggested1–4. However, other studies contend that robust organisms are more adaptable5–8. A quantitative understanding of the relationship between robustness and evolvability will help resolve these conflicting reports and will clarify outstanding problems in molecular and experimental evolution, evo-devo, and protein engineering. Using a general population-genetic model, we demonstrate here that mutational robustness can either impede or facilitate adaptation, depending on the population size, the mutation rate, and the structure of the fitness landscape. In particular, neutral diversity in a robust population can accelerate adaptation provided the number of phenotypes accessible to an individual by mutation is smaller than the total number of phenotypes in the fitness landscape. These results provide a quantitative resolution to a significant ambiguity in evolutionary theory.
A major goal of evolutionary developmental biology (evo-devo) is to understand how multicellular body plans of increasing complexity have evolved, and how the corresponding developmental programs are genetically encoded. It has been repeatedly argued that key to the evolution of increased body plan complexity is the modularity of the underlying developmental gene regulatory networks (GRNs). This modularity is considered essential for network robustness and evolvability. In our opinion, these ideas, appealing as they may sound, have not been sufficiently tested. Here we use computer simulations to study the evolution of GRNs' underlying body plan patterning. We select for body plan segmentation and differentiation, as these are considered to be major innovations in metazoan evolution. To allow modular networks to evolve, we independently select for segmentation and differentiation. We study both the occurrence and relation of robustness, evolvability and modularity of evolved networks. Interestingly, we observed two distinct evolutionary strategies to evolve a segmented, differentiated body plan. In the first strategy, first segments and then differentiation domains evolve (SF strategy). In the second scenario segments and domains evolve simultaneously (SS strategy). We demonstrate that under indirect selection for robustness the SF strategy becomes dominant. In addition, as a byproduct of this larger robustness, the SF strategy is also more evolvable. Finally, using a combined functional and architectural approach, we determine network modularity. We find that while SS networks generate segments and domains in an integrated manner, SF networks use largely independent modules to produce segments and domains. Surprisingly, we find that widely used, purely architectural methods for determining network modularity completely fail to establish this higher modularity of SF networks. Finally, we observe that, as a free side effect of evolving segmentation and differentiation in combination, we obtained in-silico developmental mechanisms resembling mechanisms used in vertebrate development.
An important question in evolutionary developmental biology is how the complex organisms we see around us have evolved, and how this complexity is encoded in their DNA. An often heard statement is that the gene regulatory networks underlying developmental processes are modular; that is, different functions are carried out by largely independent network parts. It is argued that this network modularity allows both for robust functioning and evolutionary tinkering, and that selection thus produces modular networks. Here we use a simulation model for the evolution of animal body plan patterning to investigate these ideas. To allow for the evolution of modular networks we independently select for both body plan segmentation and differentiation. We find two distinct evolutionary trajectories, one in which segments evolve before domains, and one in which segments and domains evolve simultaneously. In addition, the two evolved network types also differ in terms of developmental dynamics. We show that indirect selection for robustness favors the segments first type networks. Furthermore, as a free side effect, these more robust networks are also more evolvable. Finally, we take into account both functional and architectural aspects to determine the modularity of the network types. We show that segments simultaneous networks generate segments and domains in a integrated manner, whereas segments first networks use largely independent modules to generate segments and domains. Finally, although mimicking natural developmental mechanisms was not part of our model design, the segments first developmental mechanisms resembles vertebrate axial patterning mechanisms. This resemblance arises for free, simply from considering segmentation and differentiation in combination.
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.
In a now classic paper published in 1991, Alberch introduced the concept of genotype–phenotype (G→P) mapping to provide a framework for a more sophisticated discussion of the integration between genetics and developmental biology that was then available. The advent of evo-devo first and of the genomic era later would seem to have superseded talk of transitions in phenotypic space and the like, central to Alberch's approach. On the contrary, this paper shows that recent empirical and theoretical advances have only sharpened the need for a different conceptual treatment of how phenotypes are produced. Old-fashioned metaphors like genetic blueprint and genetic programme are not only woefully inadequate but positively misleading about the nature of G→P, and are being replaced by an algorithmic approach emerging from the study of a variety of actual G→P maps. These include RNA folding, protein function and the study of evolvable software. Some generalities are emerging from these disparate fields of analysis, and I suggest that the concept of ‘developmental encoding’ (as opposed to the classical one of genetic encoding) provides a promising computational–theoretical underpinning to coherently integrate ideas on evolvability, modularity and robustness and foster a fruitful framing of the G→P mapping problem.
modularity; developmental encoding; evolvability; genotype–phenotype mapping; robustness
Much of the current research in the growing field of evolutionary development concerns relating developmental pathways to large-scale patterns of morphological evolution, with developmental constraints on variation, and hence diversity, a field of particular interest. Tooth morphology offers an excellent model system for such ‘evo-devo’ studies, because teeth are well preserved in the fossil record, and are commonly used in phylogenetic analyses and as ecological proxies. Moreover, tooth development is relatively well studied, and has provided several testable hypotheses of developmental influences on macroevolutionary patterns. The recently-described Inhibitory Cascade (IC) Model provides just such a hypothesis for mammalian lower molar evolution. Derived from experimental data, the IC Model suggests that a balance between mesenchymal activators and molar-derived inhibitors determines the size of the immediately posterior molar, predicting firstly that molars either decrease in size along the tooth row, or increase in size, or are all of equal size, and secondly that the second lower molar should occupy one third of lower molar area. Here, we tested the IC Model in a large selection of taxa from diverse extant and fossil mammalian groups, ranging from the Middle Jurassic (~176 to 161 Ma) to the Recent.
Results show that most taxa (~65%) fell within the predicted areas of the Inhibitory Cascade Model. However, members of several extinct groups fell into the regions where m2 was largest, or rarely, smallest, including the majority of the polyphyletic “condylarths”. Most Mesozoic mammals fell near the centre of the space with equality of size in all three molars. The distribution of taxa was significantly clustered by diet and by phylogenetic group.
Overall, the IC Model was supported as a plesiomorphic developmental system for Mammalia, suggesting that mammal tooth size has been subjected to this developmental constraint at least since the divergence of australosphenidans and boreosphenidans approximately 180 Ma. Although exceptions exist, including many ‘condylarths’, these are most likely to be secondarily derived states, rather than alternative ancestral developmental models for Mammalia.
Mammalia; Developmental constraints; Teeth; Fossils
In this study we used surveys of evo-devo experts to identify the core concepts of evo-devo and outline an underlying conceptual framework. We also use interviews and surveys of conceptual difficulties with these concepts.
To examine how well biology majors have achieved the necessary foundation in evolution, numerous studies have examined how students learn natural selection. However, no studies to date have examined how students learn developmental aspects of evolution (evo-devo). Although evo-devo plays an increasing role in undergraduate biology curricula, we find that instruction often addresses development cursorily, with most of the treatment embedded within instruction on evolution. Based on results of surveys and interviews with students, we suggest that teaching core concepts (CCs) within a framework that integrates supporting concepts (SCs) from both evolutionary and developmental biology can improve evo-devo instruction. We articulate CCs, SCs, and foundational concepts (FCs) that provide an integrative framework to help students master evo-devo concepts and to help educators address specific conceptual difficulties their students have with evo-devo. We then identify the difficulties that undergraduates have with these concepts. Most of these difficulties are of two types: those that are ubiquitous among students in all areas of biology and those that stem from an inadequate understanding of FCs from developmental, cell, and molecular biology.
Classic theories of vertebrate head segmentation clearly exemplify the idealistic nature of comparative embryology prior to the 20th century. Comparative embryology aimed at recognizing the basic, primary structure that is shared by all vertebrates, either as an archetype or an ancestral developmental pattern. Modern evolutionary developmental (Evo-Devo) studies are also based on comparison, and therefore have a tendency to reduce complex embryonic anatomy into overly simplified patterns. Here again, a basic segmental plan for the head has been sought among chordates. We convened a symposium that brought together leading researchers dealing with this problem, in a number of different evolutionary and developmental contexts. Here we give an overview of the outcome and the status of the field in this modern era of Evo-Devo. We emphasize the fact that the head segmentation problem is not fully resolved, and we discuss new directions in the search for hints for a way out of this maze.
Even though pigmentation traits have had substantial impacts on the field of animal evolutionary developmental biology, they have played only relatively minor roles in plant evo-devo. This is surprising given the often direct connection between flower color and fitness variation mediated through the effects of pollinators. At the same time, ecological and evolutionary genetic studies have utilized the molecular resources available for the anthocyanin pathway to generate several examples of the molecular basis of putatively adaptive transitions in flower color. Despite this opportunity to synthesize experimental approaches in ecology, evolution, and developmental biology, the investigation of many fundamental questions in evo-devo using this powerful model is only at its earliest stages. For example, a long-standing question is whether predictable genetic changes accompany the repeated evolution of a trait. Due to the conserved nature of the biochemical and regulatory control of anthocyanin biosynthesis, it has become possible to determine whether, and under what circumstances, different types of mutations responsible for flower color variation are preferentially targeted by natural selection. In addition, because plants use anthocyanin and related compounds in vegetative tissue for other important physiological functions, the identification of naturally occurring transitions from unpigmented to pigmented flowers provides the opportunity to examine the mechanisms by which regulatory networks are co-opted into new developmental domains. Here, we review what is known about the ecological and molecular basis of anthocyanic flower color transitions in natural systems, focusing on the evolutionary and developmental features involved. In doing so, we provide suggestions for future work on this trait and suggest that there is still much to be learned from the evolutionary development of flower color transitions in nature.
anthocyanin; flower color; R2R3-MYB; predictability; co-option; pleiotropy
Cave animals are excellent models to study the general principles of evolution as well as the mechanisms of adaptation to a novel environment: the perpetual darkness of caves. In this article, two of the major model systems used to study the evolution and development (evo–devo) of cave animals are described: the teleost fish Astyanax mexicanus and the isopod crustacean Asellus aquaticus. The ways in which these animals match the major attributes expected of an evo–devo cave animal model system are described. For both species, we enumerate the regressive and constructive troglomorphic traits that have evolved during their adaptation to cave life, the developmental and genetic basis of these traits, the possible evolutionary forces responsible for them, and potential new areas in which these model systems could be used for further exploration of the evolution of cave animals. Furthermore, we compare the two model cave animals to investigate the mechanisms of troglomorphic evolution. Finally, we propose a few other cave animal systems that would be suitable for development as additional models to obtain a more comprehensive understanding of the developmental and genetic mechanisms involved in troglomorphic evolution.
The hypothesis that prenatal exposure to endocrine disruptors might cause cancer arose from challenging two well-accepted notions: (i) mammalian development is merely the unfolding of a genetic programme and (ii) only mutagenic agents can cause cancer. This hypothesis required challenging genetic determinism. The ecological developmental biology (eco-devo) movement revitalized the concept of developmental plasticity through the occurrence of polyphenisms (a single genotype produces diverse phenotypes which are determined by environmental cues). Based on the principles of eco-devo and the tissue organization field theory of carcinogenesis and neoplasia, we tested the hypothesis that exposure to xenoestrogens during foetal development in rats increased the propensity to develop mammary cancer during adulthood. We chose exposure to bisphenol A (BPA) as a model for environmental oestrogen exposure. This endocrine disruptor induced the development of ductal hyperplasias and carcinoma in situ. These highly proliferative lesions contained an increased number of oestrogen receptor α-positive cells. Thus, foetal BPA exposure was sufficient to induce the development of oestrogen-sensitive pre-neoplastic and neoplastic lesions in the mammary gland in the absence of any additional treatment aimed at increasing tumour incidence.
bisphenol A; breast cancer; endocrine disruptors; foetal exposure; mammary gland
Ovules as developmental precursors of seeds are organs of central importance in angiosperm flowers and can be traced back in evolution to the earliest seed plants. Angiosperm ovules are diverse in their position in the ovary, nucellus thickness, number and thickness of integuments, degree and direction of curvature, and histological differentiations. There is a large body of literature on this diversity, and various views on its evolution have been proposed over the course of time. Most recently evo–devo studies have been concentrated on molecular developmental genetics in ovules of model plants.
The present review provides a synthetic treatment of several aspects of the sporophytic part of ovule diversity, development and evolution, based on extensive research on the vast original literature and on experience from my own comparative studies in a broad range of angiosperm clades.
In angiosperms the presence of an outer integument appears to be instrumental for ovule curvature, as indicated from studies on ovule diversity through the major clades of angiosperms, molecular developmental genetics in model species, abnormal ovules in a broad range of angiosperms, and comparison with gymnosperms with curved ovules. Lobation of integuments is not an atavism indicating evolution from telomes, but simply a morphogenetic constraint from the necessity of closure of the micropyle. Ovule shape is partly dependent on locule architecture, which is especially indicated by the occurrence of orthotropous ovules. Some ovule features are even more conservative than earlier assumed and thus of special interest in angiosperm macrosystematics.
Angiosperms; development; diversity; evo–devo; evolution; integuments; macrosystematics; micropyle; nucellus; ovules; seed plants
In the post-genomic era, we must make maximal use of this technological advancement to broaden our perspective on biology and medicine. Our understanding of the evolutionary process is undermined by looking at it retrospectively, perpetuating a descriptive rather than a mechanistic approach. The reintroduction of developmental biologic principles into evolutionary studies, or evo-devo, allows us to apply embryologic cell-molecular biologic principles to the mechanisms of phylogeny, obviating the artificial space and time barriers between ontogeny and phylogeny. This perspective allows us to consider the continuum between the proximate and ultimate causes of speciation, which was unthinkable when looked at from the descriptive perspective. Using a cell-cell interactive ‘middle-out’ approach, we have gained insight to the evolution of the lung from the swim bladder of fish based on gene regulatory networks that generate both lung ontogeny and phylogeny, i.e. decreased alveolar size, decreased alveolar wall thickness, and increased alveolar wall strength. Vertical integration of cell-cell interactions predicts the adaptivity and maladaptivity of the lung, leading to novel insights for chronic lung disease. Since we have employed principles involved in all of development, this approach is amenable to all biologic structures, functions, adaptations, maladaptations, and diseases, providing an operational basis for preventive medicine.
MicroRNAs (miRNAs) control many important aspects of plant development, suggesting these molecules may also have played key roles in the evolution of developmental processes in plants. However, evolutionary-developmental (evo-devo) studies of miRNAs have been held back by technical difficulties in gene identification. To help solve this problem, we have developed a two-step procedure for the efficient identification of miRNA genes in any plant species. As a test case, we have studied the evolution of the MIR164 family in the angiosperms. We have identified novel MIR164 genes in three species occupying key phylogenetic positions and used these, together with published sequence data, to partially reconstruct the evolution of the MIR164 family since the last common ancestor of the extant flowering plants. We use our evolutionary reconstruction to discuss potential roles for MIR164 genes in the evolution of leaf shape and carpel closure in the angiosperms. The techniques we describe may be applied to any miRNA family and should thus enable plant evo-devo to begin to investigate the contributions miRNAs have made to the evolution of plant development.
microRNA; miR164; angiosperm; flower; carpel; leaf dissection
The origin of novel traits and their subsequent diversification represent central themes in evo-devo and evolutionary ecology. Here we explore the genetic and genomic basis of a class of traits that is both novel and highly diverse, in a group of organisms that is ecologically complex and experimentally tractable: horned beetles.
We developed two high quality, normalized cDNA libraries for larval and pupal Onthophagus taurus and sequenced 3,488 ESTs that assembled into 451 contigs and 2,330 singletons. We present the annotation and a comparative analysis of the conservation of the sequences. Microarrays developed from the combined libraries were then used to contrast the transcriptome of developing primordia of head horns, prothoracic horns, and legs. Our experiments identify a first comprehensive list of candidate genes for the evolution and diversification of beetle horns. We find that developing horns and legs show many similarities as well as important differences in their transcription profiles, suggesting that the origin of horns was mediated partly, but not entirely, by the recruitment of genes involved in the formation of more traditional appendages such as legs. Furthermore, we find that horns developing from the head and prothorax differ in their transcription profiles to a degree that suggests that head and prothoracic horns are not serial homologs, but instead may have evolved independently from each other.
We have laid the foundation for a systematic analysis of the genetic basis of horned beetle development and diversification with the potential to contribute significantly to several major frontiers in evolutionary developmental biology.
Proof of causality of most neuromental disorders (NMD's) is largely unavailable. Lessons from four-decade investigations of the epidemiology, immunology, pathogenesis, prevention and therapy of perinatal infectious agents, which invade directly the nervous system, have led us to propose a new indirect effect hypothesis: maternal transplacentally-acquired antibodies, to agents with epitope molecular mimicry with the developing nervous system, can cross the fetus/infant's blood–nervous system barriers to cause NMD's, clinically manifest years later.
Further rationale is provided by relevant evolutionary/developmental (EVO–DEVO) considerations—applicable also to some vaccines. The hypothesis is being tested in: (a) older pregnancy studies with available maternal and newborn sera, and follow-up of the progeny for NMD's; and (b) NMD registry individuals linked to their stored newborn blood spots. Preliminary results support a possible role for schizophrenia of high-tittered antibodies to some agents (toxoplasma, influenza and herpes simplex type 2 virus).
A model that includes likely genetic and postnatal influences is schematized and a list of putative agents and factors, based on varying rationales, is tabulated. In case pilot studies are confirmed, the identified agent(s) and antibodies would need to be tested in new prospectively enrolled pregnant women, so as to establish further risk factors leading to possible preventive modalities.
Robustness, maintaining a constant phenotype despite perturbations, is a fundamental property of biological systems that is incorporated at various levels of biological complexity. Although robustness has been frequently observed in nature, its evolutionary origin remains unknown. Current hypotheses suggest that robustness originated as a direct consequence of natural selection, as an intrinsic property of adaptations, or as a congruent correlate of environment robustness. To elucidate the evolutionary origins of robustness, a convenient computational package is strongly needed.
In this study, we developed the open-source integrated system EvoRSR (Evolution of RNA Structural Robustness) to explore the evolution of robustness based on biologically important landscapes induced by RNA folding. EvoRSR is object-oriented, modular, and freely available at under the GNU/GPL license. We present an overview of EvoRSR package and illustrate its features with the miRNA gene cel-mir-357.
EvoRSR is a novel and flexible package for exploring the evolution of robustness. Accordingly, EvoRSR can be used for future studies to investigate the evolution and origin of robustness and to address other common questions about robustness. While the current EvoRSR environment is a versatile analysis framework, future versions can include features to enhance evolutionary studies of robustness.
In order to broaden the comparative scope of evolutionary developmental biology and to refine our picture of animal macroevolution, it is necessary to establish new model organisms, especially from previously underrepresented groups, like the Lophotrochozoa. We have established the culture and protocols for molecular developmental biology in the rotifer species Brachionus plicatilis Müller (Rotifera, Monogononta). Rotifers are nonsegmented animals with enigmatic basal position within the lophotrochozoans and marked by several evolutionary novelties like the wheel organ (corona), the median eye, and the nonpaired posterior foot. The expression of Bp-Pax-6 is shown using whole-mount in situ hybridization. The inexpensive easy culture and experimental tractability of Brachionus as well as the range of interesting questions to which it holds the key make it a promising addition to the “zoo” of evo-devo model organisms.
Electronic supplementary material
The online version of this article (doi:10.1007/s00427-008-0234-z) contains supplementary material, which is available to authorized users.
Lophotrochozoa; Rotifer; Cleavage; Pax6
Modern sequencing technologies have massively increased the amount of data available for comparative genomics. Whole-transcriptome shotgun sequencing (RNA-seq) provides a powerful basis for comparative studies. In particular, this approach holds great promise for emerging model species in fields such as evolutionary developmental biology (evo-devo).
We have sequenced early embryonic transcriptomes of two non-drosophilid dipteran species: the moth midge Clogmia albipunctata, and the scuttle fly Megaselia abdita. Our analysis includes a third, published, transcriptome for the hoverfly Episyrphus balteatus. These emerging models for comparative developmental studies close an important phylogenetic gap between Drosophila melanogaster and other insect model systems. In this paper, we provide a comparative analysis of early embryonic transcriptomes across species, and use our data for a phylogenomic re-evaluation of dipteran phylogenetic relationships.
We show how comparative transcriptomics can be used to create useful resources for evo-devo, and to investigate phylogenetic relationships. Our results demonstrate that de novo assembly of short (Illumina) reads yields high-quality, high-coverage transcriptomic data sets. We use these data to investigate deep dipteran phylogenetic relationships. Our results, based on a concatenation of 160 orthologous genes, provide support for the traditional view of Clogmia being the sister group of Brachycera (Megaselia, Episyrphus, Drosophila), rather than that of Culicomorpha (which includes mosquitoes and blackflies).
Non-drosophilid diptera; Clogmia albipunctata; Megaselia abdita; Episyrphus balteatus; Comparative transcriptomics; RNA-seq; De novo assembly; Automated annotation; Evolutionary developmental biology; Phylogenomics
A tension has long existed between those biologists who emphasize the importance of adaptation by natural selection and those who highlight the role of phylogenetic and developmental constraints on organismal form and function. This contrast has been particularly noticeable in recent debates concerning the evolution of human language. Darwin himself acknowledged the existence and importance of both of these, and a long line of biologists have followed him in seeing, in the concept of “descent with modification”, a framework naturally able to incorporate both adaptation and constraint. Today, the integrated perspective of modern evolutionary developmental biology (“evo-devo”) allows a more subtle and pluralistic approach to these traditional questions, and has provided several examples where the traditional notion of “constraint” can be cashed out in specific, mechanistic terms. This integrated viewpoint is particularly relevant to the evolution of the multiple mechanisms underlying human language, because of the short time available for novel aspects of these mechanisms to evolve and be optimized. Comparative data indicate that many cognitive aspects of human language predate humans, suggesting that pre-adaptation and exaptation have played important roles in language evolution. Thus, substantial components of what many linguists call “Universal Grammar” predate language itself. However, at least some of these older mechanisms have been combined in ways that generate true novelty. I suggest that we can insightfully exploit major steps forward in our understanding of evolution and development, to gain a richer understanding of the principles that underlie human language evolution.
Evo-devo; Language evolution; Adaptation; Exaptation; Constraints; Spandrel; Phenotypic plasticity
Surgery has contributed to unveil a tumor behavior that is difficult to reconcile with the models of tumorigenesis based on gradualism. The postsurgical patterns of progression include unexpected features such as distant interactions and variable rhythms. The underlying evidence can be summarized as follows: (1) the resection of the primary tumor is able to accelerate the evolution of micrometastasis in early stages, and (2) the outcome is transiently opposed in advanced tumors. The objective of this paper is to give some insight into tumorigenesis and surgery-related effects, by applying the concepts of the evolutionary theory in those tumor behaviors that gompertzian and tissular-centered models are unable to explain. According to this view, tumors are the consequence of natural selection operating at the somatic level, which is the basic mechanism of tumorigenesis, notwithstanding the complementary role of the intrinsic constrictions of complex networks. A tumor is a complicated phenomenon that entails growth, evolution and development simultaneously. So, an evo-devo perspective can explain how and why tumor subclones are able to translate competition from a metabolic level into neoangiogenesis and the immune response. The paper proposes that distant interactions are an extension of the ecological events at the local level. This notion explains the evolutionary basis for tumor dormancy, and warns against the teleological view of tumorigenesis as a process directed towards the maximization of a concrete trait such as aggressiveness.
surgery; neoangiogenesis; immune system; evolution; complexity; tumor dormancy
There is a difference in viewpoint of developmental and evo-devo geneticists versus breeders and students of quantitative evolution. The former are interested in understanding the developmental process; the emphasis is on identifying genes and studying their action and interaction. Typically, the genes have individually large effects and usually show substantial dominance and epistasis. The latter group are interested in quantitative phenotypes rather than individual genes. Quantitative traits are typically determined by many genes, usually with little dominance or epistasis. Furthermore, epistatic variance has minimum effect, since the selected population soon arrives at a state in which the rate of change is given by the additive variance or covariance. Thus, the breeder's custom of ignoring epistasis usually gives a more accurate prediction than if epistatic variance were included in the formulae.
quantitave inheritance; epistasis; dominance
The diverse morphology of orchid flowers and their complex, often deceptive strategies to become pollinated have fascinated researchers for a long time. However, it was not until the 20th century that the ontogeny of orchid flowers, the genetic basis of their morphology and the complex phylogeny of Orchidaceae were investigated. In parallel, the improvement of techniques for in vitro seed germination and tissue culture, together with studies on biochemistry, physiology, and cytology supported the progress of what is now a highly productive industry of orchid breeding and propagation. In the present century both basic research in orchid flower evo-devo and the interest for generating novel horticultural varieties have driven the characterization of many members of the MADS-box family encoding key regulators of flower development. This perspective summarizes the picture emerging from these studies and discusses the advantages and limitations of the comparative strategy employed so far. I address the growing role of natural and horticultural mutants in these studies and the emergence of several model species in orchid evo-devo and genomics. In this context, I make a plea for an increasingly integrative approach.
Orchidaceae; evo-devo; MADS-box gene; peloric mutant; gene family; transcriptome; model species
Living botanical collections include germplasm repositories, long-term experimental plantings, and botanical gardens. We present here a series of vignettes to illustrate the central role that living collections have played in plant biology research, including evo-devo research. Looking toward the future, living collections will become increasingly important in support of future evo-devo research. The driving force behind this trend is nucleic acid sequencing technologies, which are rapidly becoming more powerful and cost-effective, and which can be applied to virtually any species. This allows for more extensive sampling, including non-model organisms with unique biological features and plants from diverse phylogenetic positions. Importantly, a major challenge for sequencing-based evo-devo research is to identify, access, and propagate appropriate plant materials. We use a vignette of the ongoing 1,000 Transcriptomes project as an example of the challenges faced by such projects. We conclude by identifying some of the pinch points likely to be encountered by future evo-devo researchers, and how living collections can help address them.
botanical gardens; genomics; plant developmental biology; next generation sequencing; outreach
Most evolutionary developmental biology ("evo-devo") studies of emerging model organisms focus on small numbers of candidate genes cloned individually using degenerate PCR. However, newly available sequencing technologies such as 454 pyrosequencing have recently begun to allow for massive gene discovery in animals without sequenced genomes. Within insects, although large volumes of sequence data are available for holometabolous insects, developmental studies of basally branching hemimetabolous insects typically suffer from low rates of gene discovery.
We used 454 pyrosequencing to sequence over 500 million bases of cDNA from the ovaries and embryos of the milkweed bug Oncopeltus fasciatus, which lacks a sequenced genome. This indirectly developing insect occupies an important phylogenetic position, branching basal to Diptera (including fruit flies) and Hymenoptera (including honeybees), and is an experimentally tractable model for short-germ development. 2,087,410 reads from both normalized and non-normalized cDNA assembled into 21,097 sequences (isotigs) and 112,531 singletons. The assembled sequences fell into 16,617 unique gene models, and included predictions of splicing isoforms, which we examined experimentally. Discovery of new genes plateaued after assembly of ~1.5 million reads, suggesting that we have sequenced nearly all transcripts present in the cDNA sampled. Many transcripts have been assembled at close to full length, and there is a net gain of sequence data for over half of the pre-existing O. fasciatus accessions for developmental genes in GenBank. We identified 10,775 unique genes, including members of all major conserved metazoan signaling pathways and genes involved in several major categories of early developmental processes. We also specifically address the effects of cDNA normalization on gene discovery in de novo transcriptome analyses.
Our sequencing, assembly and annotation framework provide a simple and effective way to achieve high-throughput gene discovery for organisms lacking a sequenced genome. These data will have applications to the study of the evolution of arthropod genes and genetic pathways, and to the wider evolution, development and genomics communities working with emerging model organisms.
[The sequence data from this study have been submitted to GenBank under study accession number SRP002610 (http://www.ncbi.nlm.nih.gov/sra?term=SRP002610). Custom scripts generated are available at http://www.extavourlab.com/protocols/index.html. Seven Additional files are available.]
As a result of the integration of molecular and morphological approaches for the reconstruction of phylogenies, and of the intertwining of developmental and evolutionary biology, further prospects are open for a fruitful interaction between these two fields in what we may call a phylo-evo-devo approach.
Wiegmann et al.'s molecular phylogeny of the holometabolous insect orders, recently published in BMC Biology, offers a good opportunity to revisit the inverted positions of wings and halteres in the Diptera and the Strepsiptera in terms of a putative homeotic mutation in the Hox gene Ultrabithorax. The main finding of this paper is that Strepsiptera are closely related to the Coleoptera rather than Diptera, as recently claimed. Through this exemplary case, the paper demonstrates the value of the reciprocal illumination we can expect from the integration of a good phylogeny and a sound knowledge of the evolvability of developmental mechanisms.