A general rule for the dependence of developmental rate on temperature in ectothermic animals

In animals that do not regulate their body temperature by the production of heat, the proportion of the total developmental time spent in a particular developmental stage does not change with temperature. In the quasi-linear region of the relationship between developmental rate and temperature, all of the developmental stages appear to have the same species-specific lower developmental threshold. This trait, which is called developmental isomorphy, constrains developmental adaptations of ectotherms to their environments and facilitates the precise timing of life-history events.     

Problems and terminology of functional teratology.

Possible causes for the teratogenesis of fundamental processes of life are explained. Hence, it is suggested that traditional teratology, i.e. teratomorphology (developmental pathomorphology) should be completed by teratophysiology (developmental pathophysiology), teratopsychology (developmental pathopsychology), and teratoimmunology (developmental pathoimmunology), as developmental biology can be also subdivided into developmental morphology, developmental physiology, developmental psychology and developmental immunology.     

Intrinsic and extrinsic regulators of developmental timing: from miRNAs to nutritional cues

A fundamental challenge in biology is to understand the reproducibility of developmental programs between individuals of the same metazoan species. This developmental precision reflects the meticulous integration of temporal control mechanisms with those that specify other aspects of pattern formation, such as spatial and sexual information. The cues that guide these developmental events are largely intrinsic to the organism but can also include extrinsic inputs, such as nutrition or temperature. This review discusses the well-characterized developmental timing mechanism that patterns the C. elegans epidermis. Components of this pathway are conserved, and their links to developmental time control in other species are considered, including the temporal patterning of the fly nervous system. Particular attention is given to the roles of miRNAs in developmental timing and to the emerging mechanisms that link developmental programs to nutritional cues.     

Comparative methods in developmental biology

The need for a phylogenetic framework is becoming appreciated in many areas of biology. Such a framework has found limited use in developmental studies. Our current research program is therefore directed to applying comparative and phylogenetic methods to developmental data. In this paper, we examine the concepts underlying this work, discuss potential difficulties, and identify some solutions. While developmental biologists frequently make cross-species comparisons, they usually adopt a phenetic approach, whereby degrees of overall similarity in development are sought. Little emphasis is placed on reconstructing the evolutionary divergence in developmental characters. Indeed, developmental biologists have historically concentrated on apparently ‘conserved’ or ‘universal’ developmental mechanisms. Thus, there has been little need for phylogenetic methodologies which analyse specialised features shared only within a subset of species (i.e., synapomorphies). We discuss the potential value of such methodologies, and argue that difficulties in adapting them to developmental studies fall into three interlinked areas: One concerns the nature and definition of developmental characters. Another is the difficulty of identifying equivalent developmental stages in different species. Finally the phylogenetic non-independence of developmental characters presents real problems under some protocols. These problems are not resolved. However, it is clear that the application of phylogenetic methodology to developmental data is both necessary and fundamental to research into the relationship between evolution and development.     

How to compare the lower developmental thresholds

According to the hypothesis of isomorphy rate, all the lower developmental thresholds of different developmental stages of an insect are equal. However, there is lack of a formal statistical method for testing whether there is a significant difference among the lower developmental thresholds on the basis of the traditional linear model describing developmental rate as a linear function of temperature. For comparing the lower developmental thresholds of different developmental stages, a new method based on the Chow test is proposed in the current study. Another feasible way based on the linear model proposed by Ikemoto and Takai is also proposed. The lower developmental thresholds can be compared by the analysis of covariance on this linear model. The current study can be used to test the hypothesis of isomorphy rate. When comparing the lower developmental thresholds of different geographical populations for one insect species, the two methods proposed here are also applicable.     

Developmental stability in plants: Symmetries,stress and epigenesis

Plant developmental stability has received little attention in the past three or four decades. Here we review differences in plant and animal development, and discuss the advantages of using plants as experimental subjects in exploring developmental stability. We argue that any type of developmental invariant may be used to assess developmental stability and review the use of fluctuating asymmetry in studies of plant developmental stability. We also examine the use of deviations from translatory, radial, and self-symmetry as measures of developmental instability. The role of nonlinear dynamics and epigenesis in the production of the phenotype is also discussed.     

The evolution of developmental mechanisms

Over the past two to three decades, developmental biology has demonstrated that all multicellular organisms in the animal kingdom share many of the same molecular building blocks and many of the same regulatory genetic pathways. Yet we still do not understand how the various organisms use these molecules and pathways to assume all the forms we know today. Evolutionary developmental biology tackles this problem by comparing the development of one organism to another and comparing the genes involved and gene functions to understand what makes one organism different from another. In this review, we revisit a set of seven concepts defined by Lewis Wolpert (fate maps, asymmetric division, induction, competence, positional information, determination, and lateral inhibition) that describe the characters of many developmental systems and supplement them with three additional concepts (developmental genomics, genetic redundancy, and genetic networks). We will discuss examples of comparative developmental studies where these concepts have guided observations on the advent of a developmental novelty. Finally, we identify a set of evolutionary frameworks, such as developmental constraints, cooption, duplication, parallel and convergent evolution, and homoplasy, to adequately describe the evolutionary properties of developmental systems.     

Developing the genotype-to-phenotype relationship in evolutionary theory: A primer of developmental features

For decades, there have been repeated calls for more integration across evolutionary and developmental biology. However, critiques in the literature and recent funding initiatives suggest this integration remains incomplete. We suggest one way forward is to consider how we elaborate the most basic concept of development, the relationship between genotype and phenotype, in traditional models of evolutionary processes. For some questions, when more complex features of development are accounted for, predictions of evolutionary processes shift. We present a primer on concepts of development to clarify confusion in the literature and fuel new questions and approaches. The basic features of development involve expanding a base model of genotype-to-phenotype to include the genome, space, and time. A layer of complexity is added by incorporating developmental systems, including signal-response systems and networks of interactions. The developmental emergence of function, which captures developmental feedbacks and phenotypic performance, offers further model elaborations that explicitly link fitness with developmental systems. Finally, developmental features such as plasticity and developmental niche construction conceptualize the link between a developing phenotype and the external environment, allowing for a fuller inclusion of ecology in evolutionary models. Incorporating aspects of developmental complexity into evolutionary models also accommodates a more pluralistic focus on the causal importance of developmental systems, individual organisms, or agents in generating evolutionary patterns. Thus, by laying out existing concepts of development, and considering how they are used across different fields, we can gain clarity in existing debates around the extended evolutionary synthesis and pursue new directions in evolutionary developmental biology. Finally, we consider how nesting developmental features in traditional models of evolution can highlight areas of evolutionary biology that need more theoretical attention.     

From Haeckel to event-pairing: the evolution of developmental sequences

Summary Development involves a series of developmental events, separated by transformations, that follow a particular order or developmental sequence. The sequence may in turn be arbitrarily subdivided into contiguous segments (developmental stages). We discuss the properties of developmental sequences. We also examine the differing analytical approaches that have been used to analyse developmental sequences in an evolutionary context. Ernst Haeckel was a pioneer in this field. His approach was evolutionary and he introduced the idea of sequence heterochrony (evolutionary changes in the sequence of developmental events). Despite the availability of detailed developmental data (e.g. Franz Keibel’s ‘Normal Tables’), Haeckel was unable to undertake a quantitative analysis of developmental data. This is now possible through computer-based analytical techniques such as event-pairing, which can extract important biological information from developmental sequences by mapping them onto established phylogenies. It may also yield data that can be used in phylogeny reconstruction, although the inherent ‘non-independence’ of the data may make this invalid. In future, the methods discussed here may be applied to the analysis of patterns of gene expression in embryos, or adapted to studying gene order on chromosomes.     

A topological look into the evolution of developmental programs

Rapid advance of experimental techniques provides an unprecedented in-depth view into complex developmental processes. Still, little is known on how the complexity of multicellular organisms evolved by elaborating developmental programs and inventing new cell types. A hurdle to understanding developmental evolution is the difficulty of even describing the intertwined network of spatiotemporal processes underlying the development of complex multicellular organisms. Nonetheless, an overview of developmental trajectories can be obtained from cell type lineage maps. Here, we propose that these lineage maps can also reveal how developmental programs evolve: the modes of evolving new cell types in an organism should be visible in its developmental trajectories and therefore in the geometry of its cell type lineage map. This idea is demonstrated using a parsimonious generative model of developmental programs, which allows us to reliably survey the universe of all possible programs and examine their topological features. We find that, contrary to belief, tree-like lineage maps are rare, and lineage maps of complex multicellular organisms are likely to be directed acyclic graphs in which multiple developmental routes can converge on the same cell type. Although cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs that produce low-functioning organisms. Our model indicates that additionally, lineage map topologies are correlated with such a functional property: the ability of organisms to regenerate.     

发育重塑与生物多样性

多细胞生物的成熟个体都是由单细胞的受精卵发育而来的。如果把成熟个体的表型看成生命存在的式样或模式(pattern), 那么发育就是形成和产生这种式样或模式的过程, 即塑造(patterning)或发育塑造(developmental patterning)。相应地, 对原来发育过程进行修饰或改变而产生新表型的过程就是发育重塑(developmental repatterning)。已有的研究结果表明, 发育重塑在多细胞生物的进化过程中非常普遍, 也非常重要。根据突变的类型和后果, 发育重塑既包括对相同基因在表达的时、空和量上的改变, 分别为异时(heterochrony)、异位(heterotopy)和异量(heterometry), 又包括对基因类型的改变, 即异型(heterotypy)。本文通过对一些经典案例的介绍, 揭示了发育重塑与表型变化的关系, 探讨发育重塑对生物多样性的贡献。     

Individual differences in developmental precision and fluctuating asymmetry: a model and its implications

In many studies, fluctuating asymmetry (FA) has been used as a measure of individual differences in developmental imprecision. A model of how variation in developmental imprecision is associated with variation in asymmetry is described and applied to important issues about FA. If individual differences in developmental imprecision exist, asymmetry due to developmental error should be leptokurtically distributed. Moreover, the greater the magnitude of individual differences, the greater the leptokurtosis. Asymmetry purportedly due to developmental error in a variety of species is indeed leptokurtically distributed. The level of leptokurtosis suggests that the CV in individual differences in underlying developmental imprecision is generally 20–25, consistent with it being a fitness trait. In addition, data suggest that: (1) the individual differences that underlie the developmental imprecision of different traits are largely shared across traits and not trait-specific; (2) the heritability of these individual differences may average between 35 and 55%, despite small heritabilities of individual trait FAs; and (3) correlations between FA and fitness traits or components suggest high correlations between underlying variation in developmental precision and fitness in many species. Theoretical implications are discussed.     

Testing the rate isomorphy hypothesis using five statistical methods

Abstract Organisms are said to be in developmental rate isomorphy when the proportions of developmental stage durations are unaffected by temperature. Comprehensive stage‐specific developmental data were generated on the cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), at eight temperatures ranging from 16°C to 30°C (in 2°C increments) and five analytical methods were used to test the rate isomorphy hypothesis, including: (i) direct comparison of lower developmental thresholds with standard errors based on the traditional linear equation describing developmental rate as the linear function of temperature; (ii) analysis of covariance to compare the lower developmental thresholds of different stages based on the Ikemoto‐Takai linear equation; (iii) testing the significance of the slope item in the regression line of versus temperature, where p is the ratio of the developmental duration of a particular developmental stage to the entire pre‐imaginal developmental duration for one insect or mite species; (iv) analysis of variance to test for significant differences between the ratios of developmental stage durations to that of pre‐imaginal development; and (v) checking whether there is an element less than a given level of significance in the p‐value matrix of rotating regression line. The results revealed no significant difference among the lower developmental thresholds or among the aforementioned ratios, and thus convincingly confirmed the rate isomorphy hypothesis.     

Phylogeny-based developmental analyses illuminate evolution of inflorescence architectures in dogwoods (Cornus s. l., Cornaceae)

? Inflorescence architecture is important to angiosperm reproduction, but our knowledge of the developmental basis underlying the evolution of inflorescence architectures is limited. Using a phylogeny-based comparative analysis of developmental pathways, we tested the long-standing hypothesis that umbel evolved from elongated inflorescences by suppression of inflorescence branches, while head evolved from umbels by suppression of pedicels. ? The developmental pathways of six species of Cornus producing different inflorescence types were characterized by scanning electron microscopy (SEM) and histological analysis. Critical developmental events were traced over the molecular phylogeny to identify evolutionary changes leading to the formation of umbels and heads using methods accounting for evolutionary time and phylogenetic uncertainty. ? We defined 24 developmental events describing the developmental progression of the different inflorescence types. The evolutionary transition from paniculate cymes to umbels and heads required alterations of seven developmental events occurring at different evolutionary times. ? Our results indicate that heads and umbels evolved independently in Cornus from elongated forms via an umbellate dichasium ancestor and this process involved several independent changes. Our findings shed novel insights into head and umbel evolution concealed by outer morphology. Our work illustrates the importance of combining developmental and phylogenetic data to better define morphological evolutionary processes.     

DEVELOPMENTAL STABILITY OF RAINBOW TROUT HYBRIDS: GENOMIC COADAPTATION OR HETEROZYGOSITY?

I compare the developmental stability of first generation hybrids between hatchery strains of rainbow trout (Salmo gairdneri) to that of the three pure parental strains raised in a common environment. Two of three reciprocal hybrid pairs show significantly less fluctuating asymmetry of four meristic characters than is found in parental strains. In contrast, the third hybrid pair shows reduced but not significantly lower developmental stability compared to pure strains. These hybrids had previously been found to develop slower than their maternal parental strains, indicating divergence of parental regulatory mechanisms controlling early ontogeny. A significant positive association between the degree of relative delay in hybrid developmental rate and their degree of developmental instability supports this view. For example, the only hybrid pair with decreased developmental stability also had the largest relative delay in development time of all hybrids. Neither absolute developmental rate nor enzyme heterozygosity at 42 loci alone can explain the degree of fluctuating asymmetry in these hybrids. The developmental stability of hybrids is apparently a result of the interaction between the developmental divergence between parental strains and their genomic heterozygosity due to hybridization.