A matter of measurements: challenges and approaches in the comparative analysis of static allometries

Comparisons of static allometries are frequently used to gain insights into patterns and processes underlying morphological and developmental evolution. A study by J. L. Tomkins and coworkers, recently published in the American Naturalist, examined complex nonlinear allometries in three insect species in which males are dimorphic in the expression of secondary sexual traits. Employing a novel approach to analyzing male allometries in these organisms, the authors were able to show that developmental reprogramming of trait primordia is not necessary to explain allometric scaling in two of the species examined, contrary to several previous studies on the same species. Instead, male dimorphisms could be explained by simple exponential growth, an important result that carries with it major evolutionary and developmental implications. Using this study as an example, I highlight some of the methodological challenges involved in analyzing and comparing static allometries and in inferring the developmental processes that underlie them. I end by discussing how correct application of hypothesis testing, on one side, and basic anatomy and developmental biology, on the other, should guide how morphology is measured.     

Development states associated with the floral transition.

Floral initiation can be analyzed from a developmental perspective by focusing upon how developmental fates are imprinted, remembered, and expressed. This is not an altogether new perspective, since people studying flowering have been concerned for a long time with the commitment of meristems to form flowers and the morphological, cellular, and molecular changes associated with this commitment. What is novel is the emphasis on developmental states as opposed to physiological processes. This developmental focus indicates that there appear to be at least three major developmental states that are acquired and expressed in the process of a meristem initiating floral morphogenesis. The meristem cells must first become competent to respond to a developmental signal that evokes them into a florally determined state. The leaves are the usual source of this signal and a specific leaf may or may not have the capacity to be inductively active. When a leaf does develop the capacity for inductive activity, this capacity is usually correlated with the ontogeny of the leaf. Inductive activity, however, may be continually expressed as in some day-neutral plants or may be latent as in plants where the photoperiod is the external cue for activity. Competent shoot apical meristems respond to inductive leaf signal by being evoked into a florally determined state. Under permissive conditions this florally determined state is expressed as the initiation of floral morphogenesis. Many mechanisms have evolved to regulate entry into and expression of these developmental states. As we learn more about the developmental states associated with flowering and how they are acquired and expressed, we will understand better how the various patterns of flowering are related to one another as well as which developmental processes are common to all angiosperms.     

Characterization and Expression Patterns of microRNAs Involved in Rice Grain Filling

MicroRNAs (miRNAs) are upstream gene regulators of plant development and hormone homeostasis through their directed cleavage or translational repression of the target mRNAs, which may play crucial roles in rice grain filling and determining the final grain weight and yield. In this study, high-throughput sequencing was performed to survey the dynamic expressions of miRNAs and their corresponding target genes at five distinct developmental stages of grain filling. In total, 445 known miRNAs and 45 novel miRNAs were detected with most of them expressed in a developmental stage dependent manner, and the majority of known miRNAs, which increased gradually with rice grain filling, showed negatively related to the grain filling rate. Detailed expressional comparisons revealed a clear negative correlation between most miRNAs and their target genes. It was found that specific miRNA cohorts are expressed in a developmental stage dependent manner during grain filling and the known functions of these miRNAs are involved in plant hormone homeostasis and starch accumulation, indicating that the expression dynamics of these miRNAs might play key roles in regulating rice grain filling.     

Novel and designed ecosystems

Growing attention to novel and designed ecosystems, and the confusion that follows from the overlap of these distinct ecosystem approaches, risks a loss of focus on ecological values at the core of restoration ecology. Novel ecosystems originate in ecosystems that are transformed beyond which the practical efforts of conventional restoration are feasible. They are also self‐sustaining in the sense that they take time to form, and do not typically receive regular management. In this respect, they arise differently than designed ecosystems, which are assembled with specific goals in mind and are often heavily managed. Designed (or engineered) ecosystems comprise a variety of ecological approaches including reclamation (return a degraded ecosystem to productive capacity), green infrastructure, and agroecological systems. There are three elements that distinguish novel and designed ecosystems. Designed ecosystems typically require intensive intervention to create them, and ongoing management to sustain them; novel ecosystems do not. Second, the human intentions behind designed and novel ecosystems are usually different. Designed ecosystems exist in the service of human interests, including specific services (e.g. filtration, cooling, nature appreciation), aesthetics, and shifting value commitments toward green infrastructure; novel ecosystems arise typically through inadvertent human activity. Third, designed and novel ecosystems have different developmental pathways. Historical ecosystems are the starting point for restored, hybrid, and novel ecosystems; designed ecosystems are intentionally created. Designed ecosystems stand apart as providing a new origin for ecosystems of the future, including those that become novel ecosystems.     

The zebrafish genome in context: ohnologs gone missing

Some zebrafish genes appear to lack an ortholog in the human genome and researchers often call them "novel" genes. The origin of many so-called "novel" genes becomes apparent when considered in the context of genome duplication events that occurred during evolution of the phylum Chordata, including two rounds at about the origin of the subphylum Vertebrata (R1 and R2) and one round before the teleost radiation (R3). Ohnologs are paralogs stemming from such genome duplication events, and some zebrafish genes said to be "novel" are more appropriately interpreted as "ohnologs gone missing", cases in which ohnologs are preserved differentially in different evolutionary lineages. Here we consider ohnologs present in the zebrafish genome but absent from the human genome. Reasonable hypotheses are that lineage-specific loss of ohnologs can play a role in establishing lineage divergence and in the origin of developmental innovations. How does the evolution of ohnologs differ from the evolution of gene duplicates arising from other mechanisms, such as tandem duplication or retrotransposition? To what extent do different major vertebrate lineages or different teleost lineages differ in ohnolog content? What roles do differences in ohnolog content play in the origin of developmental mechanisms that differ among lineages? This review explores these questions.     

Isolation of developmentally regulated novel genes based on sequence identity and gene expression pattern.

Based on the surmise that a variety of genes might play important roles in embryonic development and tissue differentiation, and that some of them are likely to be expressed in undifferentiated ES cells, we attempted to identify new genes from the ES cell cDNA library. The modified method of expressed sequence tags (ESTs) and the examination of the expression patterns in adult tissues and in vitro differentiated ES cells were utilized in this study. We have isolated and identified several novel cDNA clones with interesting developmental expression pattern. Among the 83 clones randomly chosen, 23 clones (27.7%) have no homology to any sequences in public databases. The rest contain limited or complete sequence homology to the previously reported mammalian genes or ESTs, yet some clones have not been previously identified in the mouse. To examine the expression profile of clones during development and differentiation, sets of slot blots were hybridized with developmental stage specific or tissue specific probes. Out of 40 novel clones tested (21 totally unknown clones and 19 unidentified clones in mouse), most of them were up- or down-regulated as differentiation proceeded, and some clones showed differentiation-stage specific expression profiles. Surprisingly, a majority of genes were also expressed in adult tissues, and some clones even revealed tissue specific expression. These results demonstrate that not only was the strategy we employed in this study quite efficient for screening novel genes, but that the information gained by such studies would also be a useful guide for further analysis of these genes. It also suggests the feasibility of this approach to explore the genomewide network of gene expression during complicated biological processes, such as embryonic development and tissue differentiation.     

Hierarchical analysis of wild Atlantic salmon (Salmo salar) fecundity in relation to body size and developmental traits

Using data from wild Atlantic salmon Salmo salar returning to spawn in seven Scottish rivers, we developed a model of fecundity based on individual body size and key developmental traits. We used a novel approach to model selection which maximises predictive accuracy for application to target river stocks to select the best from a suite of Bayesian hierarchical models. This approach aims to ensure the optimal model within the candidate set includes covariates that best predict out-of-sample data to estimate fecundity in areas where no direct observations are available. In addition to body size, the final model included the developmental characteristics of age at smolting and years spent at sea. Using two independent long-term monitoring datasets, the consequences of ignoring these characteristics was revealed by comparing predictions from the best model with models that omitted them.     

Morpholino-based gene knockdown screen of novel genes with developmental function in Ciona intestinalis

In the present study, we conducted an extensive analysis to identify novel genes with developmental function among Ciona intestinalis genes discovered by cDNA projects. Translation of a total of 200 genes expressed during embryogenesis was suppressed by using specific morpholino antisense oligonucleotides. Suppression of the translation of any of 40 genes (one-fifth of the genes tested) was thereby shown to cause specific embryonic defects. Most of these genes have counterpart(s) in mouse and human, suggesting that the present approach will be useful for identifying candidate genes essential for the development of vertebrates. Suppression of translation of 14 of these 40 genes resulted in the 'disorganized body plan' phenotype characterized by gross morphological abnormalities caused by early defects in embryogenesis. These genes encode zinc-finger, transmembrane or Pbx homeodomain proteins. The morphological features of larvae of this phenotypic class varied according to the gene suppressed, suggesting that a distinct developmental event such as tissue specification or cell cycle progression was affected in each type of larva. Suppression of the remaining 26 genes resulted in the 'abnormal tail' phenotype. Some of these genes encode proteins with known functional structures such as Zn-finger and HLH motifs. Twelve genes among them are especially interesting, because their suppression produced defects in the nervous system, as demonstrated by the loss of the sensory pigment cells or palps of the adhesive organ in the knockdown larvae. These results suggest that screening for developmental genes by the reverse genetic approach in Ciona intestinalis embryos is effective for identifying novel genes with developmental functions required for the development of chordates.     

Drosophila Heartless acts with Heartbroken/Dof in muscle founder differentiation

The formation of a multi-nucleate myofibre is directed, in Drosophila, by a founder cell. In the embryo, founders are selected by Notch-mediated lateral inhibition, while during adult myogenesis this mechanism of selection does not appear to operate. We show, in the muscles of the adult abdomen, that the Fibroblast growth factor pathway mediates founder cell choice in a novel manner. We suggest that the developmental patterns of Heartbroken/Dof and Sprouty result in defining the domain and timing of activation of the Fibroblast growth factor receptor Heartless in specific myoblasts, thereby converting them into founder cells. Our results point to a way in which muscle differentiation could be initiated and define a critical developmental function for Heartbroken/Dof in myogenesis.     

Drosophila Heartless Acts with Heartbroken/Dof in Muscle Founder Differentiation

The formation of a multi-nucleate myofibre is directed, in Drosophila, by a founder cell. In the embryo, founders are selected by Notch-mediated lateral inhibition, while during adult myogenesis this mechanism of selection does not appear to operate. We show, in the muscles of the adult abdomen, that the Fibroblast growth factor pathway mediates founder cell choice in a novel manner. We suggest that the developmental patterns of Heartbroken/Dof and Sprouty result in defining the domain and timing of activation of the Fibroblast growth factor receptor Heartless in specific myoblasts, thereby converting them into founder cells. Our results point to a way in which muscle differentiation could be initiated and define a critical developmental function for Heartbroken/Dof in myogenesis.     

Restructuring plant types for developing tailor-made crops

Plants have adapted to different environmental niches by fine-tuning the developmental factors working together to regulate traits. Variations in the developmental factors result in a wide range of quantitative variations in these traits that helped plants survive better. The major developmental pathways affecting plant architecture are also under the control of such pathways. Most notable are the CLAVATA-WUSCHEL pathway regulating shoot apical meristem fate, GID1-DELLA module influencing plant height and tillering, LAZY1-TAC1 module controlling branch/tiller angle and the TFL1-FT determining the floral fate in plants. Allelic variants of these key regulators selected during domestication shaped the crops the way we know them today. There is immense yield potential in the ‘ideal plant architecture’ of a crop. With the available genome-editing techniques, possibilities are not restricted to naturally occurring variations. Using a transient reprogramming system, one can screen the effect of several developmental gene expressions in novel ecosystems to identify the best targets. We can use the plant's fine-tuning mechanism for customizing crops to specific environments. The process of crop domestication can be accelerated with a proper understanding of these developmental pathways. It is time to step forward towards the next-generation molecular breeding for restructuring plant types in crops ensuring yield stability.     

Elements of butterfly wing patterns

The color patterns on the wings of butterflies are unique among animal color patterns in that the elements that make up the overall pattern are individuated. Unlike the spots and stripes of vertebrate color patterns, the elements of butterfly wing patterns have identities that can be traced from species to species, and typically across genera and families. Because of this identity it is possible to recognize homologies among pattern elements and to study their evolution and diversification. Individuated pattern elements evolved from non-individuated precursors by compartmentalization of the wing into areas that became developmentally autonomous with respect to color pattern formation. Developmental compartmentalization led to the evolution of serially repeated elements and the emergence of serial homology. In these compartments, serial homologues were able to acquire site-specific developmental regulation and this, in turn, allowed them to diverge morphologically. Compartmentalization of the wing also reduced the developmental correlation among pattern elements. The release from this developmental constraint, we believe, enabled the great evolutionary radiation of butterfly wing patterns. During pattern evolution, the same set of individual pattern elements is arranged in novel ways to produce species-specific patterns, including such adaptations as mimicry and camouflage.     

Pupal remodeling and the evolution and development of alternative male morphologies in horned beetles

Background  

How novel morphological traits originate and diversify represents a major frontier in evolutionary biology. Horned beetles are emerging as an increasingly popular model system to explore the genetic, developmental, and ecological mechanisms, as well as the interplay between them, in the genesis of novelty and diversity. The horns of beetles originate during a rapid growth phase during the prepupal stage of larval development. Differential growth during this period is either implicitly or explicitly assumed to be the sole mechanism underlying differences in horn expression within and between species. Here I focus on male horn dimorphisms, a phenomenon at the center of many studies in behavioral ecology and evolutionary development, and quantify the relative contributions of a previously ignored developmental process, pupal remodeling, to the expression of male dimorphism in three horned beetle species.     

Molecular and genetic regulation of fruit ripening

Fleshy fruit undergo a novel developmental program that ends in the irreversible process of ripening and eventual tissue senescence. During this maturation process, fruit undergo numerous physiological, biochemical and structural alterations, making them more attractive to seed dispersal organisms. In addition, advanced or over-ripening and senescence, especially through tissue softening and eventual decay, render fruit susceptible to invasion by opportunistic pathogens. While ripening and senescence are often used interchangeably, the specific metabolic activities of each would suggest that ripening is a distinct process of fleshy fruits that precedes and may predispose the fruit to subsequent senescence.     

DEVELOPMENTAL PROCESSES, DEVELOPMENTAL SEQUENCES AND EARLY VERTEBRATE PHYLOGENY

(1) We have put forth the position that evolutionary sequences can be deduced by an analysis of fundamental developmental sequences. Such sequences are highly conserved within a group and 'contain steps which are necessary to achieve a developmental fate'. The premise of our work then, is that such fundamental sequences do not arise de novo time and time again but can be traced back through their evolutionary history in organisms which contain portions of the sequence. (2) These highly conserved developmental sequences are in fact developmental constraints to evolution in as much as natural selection has not been able to discard them, but rather has utilized them in achieving evolutionary change. (3) We have demonstrated the ability to use developmental data by producing an evolutionary sequence for the origin of the vertebrates using the processes of neuralization and cephalization, the latter due primarily to the influences of the neural crest and epidermal placodes. The evolutionary sequence created, while not novel in structure, is distinct in that it was created solely by following a developmental sequence that is highly conserved among the vertebrates. The sequence is: (a) Chordamesoderm differentiates from the surrounding mesoderm and induces an overlying neural tube. (b) Through the influence of neuralizing morphogens, the neural tube differentiates into anterior (fore-, mid- and hindbrain) and posterior (spinal cord) parts. Cephalization has begun. (c) Cephalization proceeds via the development of two new populations of embryonic cells, the neural crest, a derivative of the neural epithelium and the epidermal placodes, derivatives of the ectoderm immediately adjacent to the neural tube. These two populations contribute significantly to the subsequent development of the vertebrate head including the skeleton, connective tissues, cranial nerve and sensory organs. Sequence (a) occurs in the most primitive protochordates and is one of the differences between the chordates and deuterostome invertebrates. Sequence (b) occurred next leading to a protochordate with a differentiated central nervous system, but lacking most vertebrate head structures. Sequence (c) signalled the beginning of the true vertebrates or branchiates (after the branchial arches which all 'vertebrates' share) since the production of a neurocranium, viscerocranium, cephalic armour, teeth and cranial peripheral ganglia was only possible with the acquisition of this developmental step.(ABSTRACT TRUNCATED AT 400 WORDS)     

Phenotypic accommodation: adaptive innovation due to developmental plasticity

Phenotypic accommodation is adaptive adjustment, without genetic change, of variable aspects of the phenotype following a novel input during development. Phenotypic accommodation can facilitate the evolution of novel morphology by alleviating the negative effects of change, and by giving a head start to adaptive evolution in a new direction. Whether induced by a mutation or a novel environmental factor, innovative morphological form comes from ancestral developmental responses, not from the novel inducing factor itself. Phenotypic accommodation is the result of adaptive developmental responses, so the novel morphologies that result are not "random" variants, but to some degree reflect past functionality. Phenotypic accommodation is the first step in a process of Darwinian adaptive evolution, or evolution by natural selection, where fitness differences among genetically variable developmental variants cause phenotype-frequency change due to gene-frequency change.     

Identification of genes encoding mouse oocyte secretory and transmembrane proteins by a signal sequence trap

The oocyte plays a key role in follicular development. At all stages of follicular development, oocytes interact with surrounding granulosa cells and promote their differentiation into the types of cells that support further oocyte growth and developmental competence. These interactions suggest the existence of an oocyte-granulosa cell regulatory loop that includes both secreted proteins and cell surface receptors on both cell types. Factors involved in the regulatory loop will therefore contain a signal sequence, which can be used to identify them through a signal sequence trap (SST). A screen of an oocyte SST library identified three classes of oocyte-expressed sequences: known mouse genes, sequences homologous to known mammalian genes, and novel sequences of unknown function. Many of the recovered genes may have roles in the oocyte-granulosa cell regulatory loop. For several of the known mouse genes, new roles in follicular development are implied by identification of their expression, for the first time, in the oocyte. The future characterization of novel sequences may lead to the identification of novel proteins participating in the regulatory loop.     

Model systems in stem cell biology

Stem cell scientists and ethicists have focused intently on questions relevant to the developmental stage and developmental capacities of stem cells. Comparably less attention has been paid to an equally important set of questions about the nature of stem cells, their common characteristics, their non-negligible differences and their possible developmental species specificity. Answers to these questions are essential to the project of justly inferring anything about human stem cell biology from studies in non-human model systems--and so to the possibility of eventually developing human therapies based on stem cell biology. After introducing and discussing these questions, I conclude with a brief discussion of the creation of novel model systems in stem cell biology: human-to-animal embryonic chimeras. Such novel model systems may help to overcome obstacles to extrapolation, but they are also scientifically and ethically contentious.