The evolutionary and morphological history of the parasphenoid bone in vertebrates

The parasphenoid is located in the cranium of many vertebrates. When present, it is always an unpaired, dermal bone. While most basal vertebrates have a parasphenoid, most placental mammals lack this element and have an unpaired, dermal vomer in a similar position (i.e. associated with the same bones) and with a similar function. As such, the parasphenoid and the vomer were considered homologous by some early twentieth century researchers. However, others questioned this homology based on comparisons between mammals and reptiles. Here we investigate the parasphenoid bone across the major vertebrate lineages (amphibians, reptiles, mammals and teleosts) including both developmental and evolutionary aspects, which until now have not been considered together. We find that within all the major vertebrate lineages there are organisms that possess a parasphenoid and a vomer, while the parasphenoid is absent within caecilians and most placental mammals. Based on our assessment and Patterson's conjunction tests, we conclude that the non‐mammalian parasphenoid and the vomer in mammals cannot be considered homologous. Additionally, the parasphenoid is likely homologous between sarcopterygian and actinopterygian lineages. This research attempts to resolve the issue of the parasphenoid homology and highlights where gaps in our knowledge are still present.     

Evolution of insect wings and development – new details from Palaeozoic nymphs

The nymphal stages of Palaeozoic insects differ significantly in morphology from those of their modern counterparts. Morphological details for some previously reported species have recently been called into question. Palaeozoic insect nymphs are important, however – their study could provide key insights into the evolution of wings, and complete metamorphosis. Here we review past work on these topics and juvenile insects in the fossil record, and then present both novel and previously described nymphs, documented using new imaging methods. Our results demonstrate that some Carboniferous nymphs – those of Palaeodictyopteroidea – possessed movable wing pads and appear to have been able to perform simple flapping flight. It remains unclear whether this feature is ancestral for Pterygota or an autapomorphy of Palaeodictyopteroidea. Further characters of nymphal development which were probably in the ground pattern of Pterygota can be reconstructed. Wing development was very gradual (archimetaboly). Wing pads did not protrude from the tergum postero‐laterally as in most modern nymphs, but laterally, and had well‐developed venation. The modern orientation of wing pads and the delay of wing development into later developmental stages (condensation) appears to have evolved several times independently within Pterygota: in Ephemeroptera, Odonatoptera, Eumetabola, and probably several times within Polyneoptera. Selective pressure appears to have favoured a more pronounced metamorphosis between the last nymphal and adult stage, ultimately reducing exploitation competition between the two. We caution, however, that the results presented herein remain preliminary, and the reconstructed evolutionary scenario contains gaps and uncertainties. Additional comparative data need to be collected. The present study is thus seen as a starting point for this enterprise.     

Hydra and the evolution of stem cells

Hydra are remarkable because they are immortal. Much of immortality can be ascribed to the asexual mode of reproduction by budding, which requires a tissue consisting of stem cells with continuous self‐renewal capacity. Emerging novel technologies and the availability of genomic resources enable for the first time to analyse these cells in vivo. Stem cell differentiation in Hydra is governed through the coordinated actions of conserved signaling pathways. Studies of stem cells in Hydra, therefore, promise critical insights of general relevance into stem cell biology including cellular senescence, lineage programming and reprogramming, the role of extrinsic signals in fate determination and tissue homeostasis, and the evolutionary origin of these cells. With these new facts as a backdrop, this review traces the history of studying stem cells in Hydra and offers a view of what the future may hold.     

The uropygial gland of the monk parakeet Myiopsitta monachus: Histology,morphogenesis, and evolution within Psittaciformes (Aves)

We describe the morphology, histology, and histochemical characteristics of the uropygial gland (UG) of the monk parakeet Myiopsitta monachus. The UG has a heart‐shape external appearance and adenomers extensively branched with a convoluted path, covered by a stratified epithelium formed by different cellular strata and divided into three zones (based on the epithelial height and lumen width), a cylindrical papilla with an internal structure of delicate type and two excretory pores surrounded by a feather tuft. Histochemical and lectin‐histochemical techniques performed showed positivity against PAS, AB pH 2.5, AB‐PAS, and some lectines, likely related to the granivorous feeding habits. Also, we describe the morphogenesis of the UG of the monk parakeet, which appears at embryological stage 34 as a pair of ectodermal invaginations. Heterochronic events in the onset development of the UG when compared with other birds could be recognized. Finally, to examine the phylogenetic occurrence of the UG within the Psittaciformes and infer its evolutionary history, we mapped its presence/absence over a molecular phylogeny. The reconstruction of the characters states at ancestral nodes revealed that the presence of the UG was the plesiomorphic feature for Psittaciformes and its loss evolved independently more than once.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

Flower morphology and relationships of Schefflera subintegra (Araliaceae,Apiales): an evolutionary step towards extreme floral polymery

Gross morphology and the development of flowers in Schefflera subintegra (Araliaceae) are examined. The floral groundplan of this species is found to be very similar to that of Tupidanthus calyptratus representing a case of most extreme floral polymery within Araliaceae. Schefflera subintegra differs from T. calyptratus with respect to a lower floral merism (19–43 versus 60–172 stamens and 15–33 versus 60–138 carpels respectively) and by transformation from polysymmetry to disymmetry of flower in the course of its development. Close relationships between S. subintegra, T. calyptratus, and Schefflera hemiepiphytica have been confirmed by phylogenetic analysis based on nuclear ribosomal internal transcribed spacer sequences. These species form a subclade within the Asian Schefflera clade, with T. calyptratus as a sister taxon to two other species. Apart from more or less pronounced floral polymery, the species of this subclade share calyx and corolla without any traits of individual sepals and petals, and also a massive calyptra. As these data suggest, the extremely polymerous flowers of Tupidanthus apparently evolved in two steps: (1) the saltational multiplication of floral elements together with a loss of individuality of sepals in the calyx and petals in the corolla and (2) further polymerization of androecium and gynoecium. Mutation(s) in CLAVATA‐like gene(s) are suggested as a possible mechanism of the saltation event. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175 , 553–597.     

Roles for modularity and constraint in the evolution of cranial diversity among Anolis lizards

Complex organismal structures are organized into modules, suites of traits that develop, function, and vary in a coordinated fashion. By limiting or directing covariation among component traits, modules are expected to represent evolutionary building blocks and to play an important role in morphological diversification. But how stable are patterns of modularity over macroevolutionary timescales? Comparative analyses are needed to address the macroevolutionary effect of modularity, but to date few have been conducted. We describe patterns of skull diversity and modularity in Caribbean Anolis lizards. We first diagnose the primary axes of variation in skull shape and then examine whether diversification of skull shape is concentrated to changes within modules or whether changes arose across the structure as a whole. We find no support for the hypothesis that cranial modules are conserved as species diversify in overall skull shape. Instead we find that anole skull shape and modularity patterns independently converge. In anoles, skull modularity is evolutionarily labile and may reflect the functional demands of unique skull shapes. Our results suggest that constraints have played little role in limiting or directing the diversification of head shape in Anolis lizards.     

How a growing organismal perspective is adding new depth to integrative studies of morphological evolution

Over the past half century, the field of Evolutionary Developmental Biology, or Evo‐devo, has integrated diverse fields of biology into a more synthetic understanding of morphological diversity. This has resulted in numerous insights into how development can evolve and reciprocally influence morphological evolution, as well as generated several novel theoretical areas. Although comparative by default, there remains a great gap in our understanding of adaptive morphological diversification and how developmental mechanisms influence the shape and pattern of phenotypic variation. Herein we highlight areas of research that are in the process of filling this void, and areas, if investigated more fully, that will add new insights into the diversification of morphology. At the centre of our discussion is an explicit awareness of organismal biology. Here we discuss an organismal framework that is supported by three distinct pillars. First, there is a need for Evo‐devo to adopt a high‐resolution phylogenetic approach in the study of morphological variation and its developmental underpinnings. Secondly, we propose that to understand the dynamic nature of morphological evolution, investigators need to give more explicit attention to the processes that generate evolutionarily relevant variation at the population level. Finally, we emphasize the need to address more thoroughly the processes that structure variation at micro‐ and macroevolutionary scales including modularity, morphological integration, constraint, and plasticity. We illustrate the power of these three pillars using numerous examples from both invertebrates and vertebrates to emphasize that many of these approaches are already present within the field, but have yet to be formally integrated into many research programs. We feel that the most exciting new insights will come where the traditional experimental approaches to Evo‐devo are integrated more thoroughly with the principles of this organismal framework.     

A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology

Vertebrate developmental biologists typically rely on a limited number of model organisms to understand the evolutionary bases of morphological change. Unfortunately, a typical model system for squamates (lizards and snakes) has not yet been developed leaving many fundamental questions about morphological evolution unaddressed. New model systems would ideally include clades, rather than single species, that are amenable to both laboratory studies of development and field-based analyses of ecology and evolution. Combining an understanding of development with an understanding of ecology and evolution within and between closely related species has the potential to create a seamless understanding of how genetic variation underlies ecologically and evolutionarily relevant variation within populations and between species. Here we briefly introduce a new model system for the integration of development, evolution, and ecology, the lizard genus Anolis, a diverse group of lizards whose ecology and evolution is well understood, and whose genome has recently been sequenced. We present a developmental staging series for Anolis lizards that can act as a baseline for later comparative and experimental studies within this genus.     

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.     

Empowering plant evo-devo: virus induced gene silencing validates new and emerging model systems

It is increasingly recognized that current established model systems are not sufficient to understand the evolution of biodiversity. The main limitation in developing additional model systems is the difficulty or inability to perform functional studies of target genes. Evolutionary developmental (evo-devo) biologists have adopted a transient transgenic technique, developed over the last decade for agricultural applications, which is allowing functional studies in the most disparate plant lineages. From monocots to dicots and from herbs to trees, virus-induced gene silencing (VIGS) has opened up a world of opportunities in plant evo-devo.     

Plant‐microbe symbioses: new insights into common roots

Arbuscular mycorrhiza (AM), a type of plant‐fungal endosymbiosis, and nodulation, a bacterial‐plant endosymbiosis, are the most ubiquitous symbioses on earth. Recent findings have established part of a shared genetic basis underlying these interactions. Here, we approach root endosymbioses through the lens of the homology and modularity concepts aiming at further clarifying the proximate and ultimate causes for the establishment of these biological systems. We review the genetics that underlie interspecific signaling and its concomitant shift in genetic programs for either partner. Also, through the comparative analysis of genetic modules shared by AM and nodulation symbioses, we identify fundamental nodes in these networks, suggesting the elemental steps that may have permitted symbiotic adaptation. Here, we show that this approach, allied to recent technical advances in the study of genetic systems architecture, can provide clear testable hypotheses for the advancement of our understanding on the evolution and development of symbiotic systems.     

Chironomid midges: a forgotten model of developmental biology research

For more than a century, embryologists have been exploring various model systems to gain insights into developmental processes. This article presents an overview of the role of chironomid midges in embryology research since their introduction as model organisms in the 19th century. We present the vestiges of bibliography since the days of Weismann (1834–1914), who raised preliminary queries to unravel many unique features of insect embryogenesis using midges as a crucible. Unfortunately, over the years, chironomid midges got lost into obscurity as a model for developmental biology, which is evident from the paucity of developmental biology–related literature on midges in the past decades. Through this essay, the authors intend to share reminiscences of the heydays of chironomid research with the wider community of zoologists with an aim of reviving chironomid embryology. Midges not only possess the basic qualities essential for an ideal model system, but being one of the ancestral dipteran stocks, they can also prove an excellent test system for evo‐devo, transgenetic, and embryogenomic investigations that utilize methodologies at the interface of developmental biology and high‐throughput molecular genetic and genomics approach. An introspection of re‐introducing chironomid midgesas model system will be rewarding for the contemporary developmental biologists.     

Evolutionary stasis in Euphorbiaceae pollen: selection and constraints

Although much attention has been paid to the role of stabilizing selection, empirical analyses testing the role of developmental constraints in evolutionary stasis remain rare, particularly for plants. This topic is studied here with a focus on the evolution of a pollen ontogenetic feature, the last points of callose deposition (LPCD) pattern, involved in the determination of an adaptive morphological pollen character (aperture pattern). The LPCD pattern exhibits a low level of evolution in eudicots, as compared to the evolution observed in monocots. Stasis in this pattern might be explained by developmental constraints expressed during male meiosis (microsporogenesis) or by selective pressures expressed through the adaptive role of the aperture pattern. Here, we demonstrate that the LPCD pattern is conserved in Euphorbiaceae s.s. and that this conservatism is primarily due to selective pressures. A phylogenetic association was found between the putative removal of selective pressures on pollen morphology after the origin of inaperturate pollen, and the appearance of variation in microsporogenesis and in the resulting LPCD pattern, suggesting that stasis was due to these selective pressures. However, even in a neutral context, variation in microsporogenesis was biased. This should therefore favour the appearance of some developmental and morphological phenotypes rather than others.     

The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus: The establishment of a new chelicerate model system

Summary: Chelicerates, which include spiders, ticks, mites, scorpions, and horseshoe crabs, are members of the phylum Arthropoda. In recent years, several molecular experimental studies of chelicerates have examined the embryology of spiders; however, the embryology of other groups, such as ticks (Acari: Parasitiformes), has been largely neglected. Ticks and mites are believed to constitute a monophyletic group, the Acari. Due to their blood‐sucking activities, ticks are also known to be vectors of several diseases. In this study, we analyzed the embryonic development of the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). First, we developed an embryonic staging system consisting of 14 embryonic stages. Second, histological analysis and antibody staining unexpectedly revealed the presence of a population of tick cells with similar characteristics to the spider cumulus. Cumulus cell populations also exist in other chelicerates; these cells are responsible for the breaking of radial symmetry through bone morphogenetic protein signaling. Third, it was determined that the posterior (opisthosomal) embryonic region of R. microplus is segmented. Finally, we identified the presence of a transient ventral midline furrow and the formation and regression of a fourth leg pair; these features may be regarded as hallmarks of late tick embryogenesis. Importantly, most of the aforementioned features are absent from mite embryos, suggesting that mites and ticks do not constitute a monophyletic group or that mites have lost these features. Taken together, our findings provide fundamental common ground for improving knowledge regarding tick embryonic development, thereby facilitating the establishment of a new chelicerate model system. genesis 51:803–818. © 2013 Wiley Periodicals, Inc.