Sequence Of Developmental Events Research Articles

Variation and Variability in Skeletal Ossification of the Gray Short-tailed Opossum, Monodelphis domestica.

By reconstructing and comparing the sequence of ontogenetic (embryonic development and post-natal growth) events across species, developmental biologists have gained unique insights into the key processes underlying the evolution of modern lineages and their extinct relatives. However, despite the importance of intraspecific variation to evolutionary transformation and lineage divergence, variation in the sequence of developmental events is seldom acknowledged. Thus, how much variation or variability should be expected during ontogeny remains poorly understood and it is an open question to what extent it impacts interspecific comparisons of developmental patterns. To address this crucial question, we studied the skeletal development of the important biomedical and developmental model organism, Monodelphis domestica. We investigated cranial, forelimb, and hindlimb elements using ontogenetic sequence analysis (OSA) to quantify and assess the full range of variation and variability in the sequence of ossification. Our study documented that previously unrecognized variation exists during M. domestica ontogeny-with over 5000 sequences for the full 92 event analysis. Further, OSA revealed unexpectedly high variability (i.e., the propensity to express variation) in the sequence of ossification for the skull and across the entire skeleton. Reconstructed modal sequences were generally in agreement with previously recognized patterns, including earlier ossification of the facial skeleton and a slight offset between forelimb and hindlimb development. However, the full range of variation shows that the majority of specimens in our analysis followed developmental trajectories distinct from those recovered by prior studies. This level of variation is quite remarkable and demonstrates the importance of assessing intraspecific ontogenetic variation. By quantifying sequence polymorphism and studying how developmental variation and variability differ among species, we can clarify more precisely how developmental patterns differ among species and gain insights into how ontogeny itself evolves.

Patterns of allometric and heterochronic changes in the early ontogeny of species of Physalaemus (Anura: Leptodactylidae).

We studied the relationship between shape, size, and developmental time in the embryonic ontogeny of 15 species of the frog genus Physalaemus. As in other anuran exotrophic embryos, shape changes are correlated with size increase and mainly concern tail elongation, decrease in body height, and increase in fin height. Size ranges and developmental times vary interspecifically. Embryos of the P. signifer Clade and the P. gracilis Group are among the largest, are slightly peramorphic, and develop fast regarding congeneric species. Embryos of P. cicada combine the smallest sizes with fast development and the most peramorphic shapes. The paedomorphic shapes of embryos of P. biligonigerus and P. henselii groups are correlated with fast vs. slow developmental times respectively. Trajectories in the P. cuvieri Group are diverse and in general differ in size and developmental time. The embryos of P. cristinae and from the Argentinean lineage of P. cuvieri stand out with the longest development. Sequences of developmental events are overall conserved in the genus, and main differences concern mouthpart ontogeny. This study constitutes the first attempt to evaluate morphological, allometric, and heterochronic parameters of the early ontogeny of anurans and how these can vary and contribute to diversification in taxonomic groups.

Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification.

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony-based methods-event-pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event-dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.

Suggested mechanisms underlying pollen wall development in Ambrosia trifida (Asteraceae: Heliantheae).

By a detailed ontogenetic study of Ambrosia trifida pollen, tracing each stage of development with TEM, we aim to understand the establishment of the pollen wall and to unravel the mechanisms underlying sporoderm development. The main steps of exine ontogeny in Ambrosia trifida, observed in the microspore periplasmic space, are as follows: spherical units, gradually transforming into columns, then to rod-like units; the appearance of the initial reticulate tectum; growth of columellae under the tectum and initial sporopollenin accumulation on them; the appearance of the endexine lamellae, first in fragments, then in long laminae; the cessation of the glycocalyx growth and its detachment from the plasma membrane, resulting in the appearance of gaps; massive accumulation of sporopollenin on the tectum, columellae, and endexine, and the appearance of the foot layer at the young post-tetrad stage, accompanied by establishment of caveae in sites of the former gaps; and final massive sporopollenin accumulation. This sequence of developmental events in all probability corresponds to the sequence of self-assembling micellar mesophases. This gives (together with earlier findings and experimental modeling of exine) strong evidence that the genome and self-assembly share control of exine formation. In this sense, self-assembly itself can be seen as an inherent mechanism of evolution.

The ontogeny of the lower reproductive tract of the landsnail Helix aspersa (Gastropoda: Mollusca)

We provide a size-based ontogenetic sequence of the development and differentiation of the lower reproductive tract of the heterobranch gastropod Helix aspersa (Muller 1774). Twelve development stages distributed among nine size classes were recognized based on readily visible changes in morphology and changes in tissue density. Geometric morphometrics was used to calculate the deformation between stages as represented by thin-plate spline bending energies. The developmental stages and sequence of developmental events are also compared to previously published scenarios for the evolution of stylommatophoran and other pulmonate reproductive tracts. These comparisons suggest that heterochronies, which include both acceleration and retardation, are operating in the morphological evolution of the pulmonate lower reproductive tract. This supports previous observations that largest number of developmental changes coincides with the transition to sexual maturity, which is also seen in the exponential curve of bending energies we observed in Helix aspersa. The belated organogenesis makes the ontogeny of the complex hermaphroditic reproductive system of pulmonates readily observable in size-friendly juveniles. This observation, coupled with the ease of raising individuals in the laboratory, recommends Helix aspersa as a potential model laboratory system for investigating molluscan evolutionary development.

A genetic basis for intraspecific differences in developmental timing?

Heterochrony, altered developmental timing between ancestors and their descendents, has been proposed as a pervasive evolutionary feature and recent analytical approaches have confirmed its existence as an evolutionary pattern. Yet, the mechanistic basis for heterochrony remains unclear and, in particular, whether intraspecific variation in the timing of developmental events generates, or has the potential to generate, future between-species differences. Here we make a key step in linking heterochrony at the inter- and intraspecific level by reporting an association between interindividual variation in both the absolute and relative timing (position within the sequence of developmental events) of key embryonic developmental events and genetic distance for the pond snail, Radix balthica. We report significant differences in the genetic distance of individuals exhibiting different levels of dissimilarity in their absolute and relative timing of developmental events such as spinning activity, eyespot formation, heart ontogeny, and hatching. This relationship between genetic and developmental dissimilarity is consistent with there being a genetic basis for variation in developmental timing and so suggests that intraspecific heterochrony could provide the raw material for natural selection to produce speciation.

Environmentally Cued Hatching across Taxa: Embryos Respond to Risk and Opportunity

Most animals begin life in eggs, protected and constrained by a capsule, shell, or other barrier. As embryos develop, their needs and abilities change, altering the costs and benefits of encapsulation, and the risks and opportunities of the outside world. When the cost/benefit ratio is better outside the egg, animals should hatch. Adaptive timing of hatching evolves in this context. However, many environmental variables affect the optimal timing of hatching so there is often no consistent best time. Across a broad range of animals, from flatworms and snails to frogs and birds, embryos hatch at different times or at different developmental stages in response to changing risks or opportunities. Embryos respond to many types of cues, assessed via different sensory modalities. Some responses appear simple. Others are surprisingly complex and sophisticated. Parents also manipulate the timing of hatching. The number and breadth of examples of cued hatching suggest that, in the absence of specific information, we should not assume that hatching timing is fixed. Our challenge now is to integrate information on the timing of hatching across taxa to better understand the diversity of patterns and how they are structured in relation to different types of environmental and developmental variation. As starting points for comparative studies, I: (1) suggest a framework based on heterokairy-individual, plastic variation in the rate, timing, or sequence of developmental events and processes-to describe patterns and mechanisms of variation in the timing of hatching; (2) briefly review the distribution of environmentally cued hatching across the three major clades of Bilateria, highlighting the diverse environmental factors and mechanisms involved; and (3) discuss factors that shape the diversity of plastic and fixed timing of hatching, drawing on evolutionary theory on phenotypic plasticity which directs our attention to fitness trade-offs, environmental heterogeneity, and predictive cues. Combining mechanistic and evolutionary perspectives is necessary because development changes organismal interactions with the environment. Integrative and comparative studies of the timing of hatching will improve our understanding of embryos as both evolving and developing organisms.

Brief communication: Methods of sequence heterochrony for describing modular developmental changes in human evolution

Interest in the developmental changes leading to apomorphic features of human anatomy is longstanding. Although most research has focused on quantitative measures of size and shape, additional information may be available in the sequence of events in development, including aspects of phenotypic integration. I apply two recently proposed techniques for analyzing developmental sequences to literature data on human and chimpanzee age of limb element ossification center appearance in radiographs. The event-pair cracking method of Jeffery et al. (Syst Biol 51 [2002] 478-491) offers little additional insight on sequence differences in this data set than a simpler difference of ranks. Both reveal shifts in timing that are likely related to locomotor differences between the two species. Poe's (Evolution 58 [2004] 1852-1855) test for modularity in a sequence identifies the ankle, wrist, and hind limb as developmental modules, which may correspond to localized combinations of developmental genes. Ossification patterns of the rays of the hand and foot show little modularity. Integrating these and other methods of sequence analysis with traditional metrics of size and shape remains an underdeveloped area of inquiry.

Methods for the analysis of developmental sequence data

Heterochrony, evolutionary changes in developmental timing, can be studied either by examining changes in growth or changes in the sequence of developmental events. Developmental sequence data has the potential to address many important questions in the field of developmental evolution, but methodological challenges remain due to the biological and logical dependence of events in a ranked sequence. In the past 10 years, the study of sequence heterochrony has undergone a rebirth, with the creation of several new methods for the analysis of this type of data. These methods can be divided into two broad categories: phenetic comparisons between terminal taxa that strive to uncover integrations within the developmental sequences and putative shared sequence heterochronies, and phylogeny-based methods that derive ancestor-descendent sequence heterochronies and establish statements of sequence evolution. In this review, we will discuss the strengths and weaknesses of the methodologies that have been proposed to quantitatively examine developmental sequence data, and studies that have attempted to implement them in an evolutionary context.

PHYSIOLOGICAL REACTIONS OF LILIES DURING COLD STORAGE IN VITRO

Induction of dormancy with subsequent cold incubation is important for maintaining the natural sequence of developmental events during production of lily bulblets by means of tissue culture. The present study was initiated to test a possibility of using enzyme activities as biochemical markers for morphogenic capacity and viability of lily bulblets as affected by the duration of pretreatment period and carbohydrate content in the cultivation medium. Bulblet quality was affected both by the length of period for dormancy induction as well as by the concentration of sucrose in the medium. Pretreatment period of 21 days together with increased sucrose concentration (4-6%) gave the best results yielding bulblets of high quality with well- developed roots after two months of cold storage. Activities of peroxidase and catalase were inversed to the quality of bulblets, peroxidase activity being more characteristic indicator.

Heterochronic genes

What does the term heterochronic mean? Heterochronic refers to the development of cells or tissues at an abnormal time relative to other unaffected events in an organism; the latter can thus serve as temporal landmarks. Mutations in heterochronic genes cause certain cells to adopt cell fates normally associated with earlier or later times in development. Heterochronic genes therefore regulate the timing and sequence of developmental events in specific cell lineages, and thereby coordinate events throughout a developing organism. Why study heterochronic genes in worms? The nematode Caenorhabditis elegans provides a particularly tractable model for studying heterochronic genes, owing to its relatively simple and invariant cell lineages. In the four larval stages of its post-embryonic development, C. elegans cells exhibit stage-specific patterns of developmental events, such as cell division and cell fate specification, with each stage separated by a molt. Importantly, neither larval growth nor progression through the molting cycle in the worm are affected by known heterochronic mutations, allowing developmental events to be monitored relative to these temporal landmarks. So, is this just a strange worm phenomenon? No. Heterochronic genes have been reported in many different organisms, including Drosophila (hunchback, Krüppel, pdm, castor) and several species of plants, including Arabidopsis (HASTY) and rice (mori1). What do heterochronic genes do in worms? One class of heterochronic mutations results in an early, or precocious, phenotype in which many of the normal cell fate decisions of a specific larval stage are skipped and much of the worm instead executes the developmental program of a later stage. Examples include mutations in lin-14, lin-28 and lin-41. Worms with such mutations express adult cell fates when the animal is still sexually immature (Figure 1). Conversely, a second class of mutations results in a delayed, or retarded, phenotype in which many normal cell fate decisions are reiterated in subsequent larval stages. Examples include mutations in lin-4 and lin-29. Worms with such mutations do not express certain adult cell fates, despite being sexually mature (Figure 1). Is there conservation in heterochronic gene pathways? An important regulator of the larval-to-adult transition in worms, let-7, is conserved across diverse phyla, having been identified in flies, sea urchins, humans and many other organisms. In addition, it has recently been demonstrated that the C. elegans heterochronic gene lin-57 is a worm homolog of the Drosophila gene hunchback (hence its new name hbl-1). In the developing central nervous system of flies, hunchback regulates the temporal patterning of cell fate specification for neuroblasts. But doesn't hunchback regulate spatial patterning in flies?Hunchback is indeed best known for its role in anterior–posterior patterning in the early fly embryo; it encodes a zinc-finger transcription factor that acts to establish spatial domains of gene expression. Although downstream effectors are unknown in worms, it is possible that hbl-1 is able to establish analogous temporal domains of gene expression. What's the deal with microRNAs and how are they involved in the heterochronic gene pathway? microRNAs are now appreciated as a new class of small non-coding RNAs. They are likely to act by regulating translation of target mRNAs through binding to sequences in the 3′ untranslated regions with partial anti-sense complementarity. When the product of the lin-4 heterochronic gene was found to be a small, non-coding RNA in 1993, it appeared that it might be a C. elegans-specific, molecular oddity. A second small non-coding RNA, let-7, was discovered in the heterochronic gene pathway in 2000, followed by the cloning of hundreds of small non-coding RNAs (microRNAs) in 2001 and beyond, and it is now appreciated that the heterochronic genes lin-4 and let-7 are the founding members of a larger microRNA gene family. Are microRNAs involved in other pathways? Although the first two microRNAs identified are in the heterochronic gene pathway, there is now evidence for roles of microRNAs in cell proliferation, cell death, fat metabolism and stress resistance in flies. Is there anything we don't know? The mechanism of action of many heterochronic genes remains to be determined. For example, lin-14 encodes a novel nuclear protein with no identified downstream effectors to date. In addition, emerging evidence of phylogenetic conservation of heterochronic genes leads to the prospect that mechanisms to control developmental timing will be elucidated in other systems. Where can I find out more?

Genetics and hypogonadotrophic hypogonadism.

Hypothalamic pulsatile gonadotrophin-releasing hormone secretion, stimulating pituitary gonadotrophin secretion, is essential for adult reproductive function. This neuroendocrine drive to the reproductive axis is critically dependent on a sequence of developmental events in utero. During early foetal life, gonadotrophin-releasing hormone neurones migrate from the nasal placode to the medial basal hypothalamus where gonadotrophin-releasing hormone can be transported down portal vessels to the anterior pituitary. Gonadotrophin-releasing hormone secretion is active fleetingly neonatally but soon becomes quiescent throughout childhood. At the time of puberty activation of gonadotrophin-releasing hormone secretion reawakens the hypothalamic pituitary-gonadal axis and secondary sexual maturation is triggered. Any disruption in gonadotrophin-releasing hormone secretion will result in hypogonadotrophic hypogonadism. The clinical manifestations of this become apparent with secondary sexual maturation. Genetic mutations have been identified in a minority of cases. These include Kallmann syndrome, adrenal hypoplasia congenital, gonadotropin-releasing hormone receptor and luteinizing hormone or follicle-stimulating hormone beta-subunit gene mutations. The importance of these discoveries is important not only in relation to the conditions that result, but also for our better understanding of normal reproductive function.

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

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.

Sequential Docking, Molecular Differentiation, and Positioning of T-Tubule/SR Junctions in Developing Mouse Skeletal Muscle

Skeletal muscle Ca2+ release units (CRUs) are junctions of the surface membrane/T-tubule system and the sarcoplasmic reticulum (SR) that function in excitation–contraction coupling. They contain high concentrations of dihydropyridine receptors (DHPRs) in the T-tubules and of ryanodine receptors (RyR) in the SR and they are positioned at specific locations in the sarcomere. In order to characterize the sequence of developmental steps leading to the specific molecular and structural organization of CRUs, we applied a range of imaging techniques that allowed us to follow the differentiation of the membrane compartments and the expression of junctional proteins in developing mouse diaphragm muscle. We find that docking of the two membrane systems precedes the incorporation of the RyRs into the junctions, and that T-tubule/SR junctions are formed and positioned at the I-A interface at a stage when the orientation of T-tubule is predominantly longitudinal. Thus, the sequence of developmental events is first the docking of T-tubules and SR, secondly the incorporation of RyR in the junctions, thirdly the positioning of the junctions in the sarcomere, and only much later the transverse orientation of the T-tubules. These sequential stages suggests an order of inductive processes for the molecular differentiation and structural organization of the CRUs in skeletal muscle development.

Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

SummaryIn nature, larvae of the dung beetle Onthophagus taurus (Schreber 1759) are confronted with significant variation in the availability of food without the option of locating new resources. Here we explore how variation in feeding conditions during the final larval instar affects larval growth and the timing of pupation. We found that larvae respond to food deprivation with a reduction in the length of the instar and premature pupation, leading to the early eclosion of a small adult. To achieve pupation, larvae required access to food for at least the first 5 days of the final instar (= 30% of mean third‐instar duration in control individuals), and had to exceed a weight of 0.08 g (= 58% of mean peak weight in control individuals). Larvae that were allowed to feed longer exhibited higher pupation success, but increased larval weight at the time of food deprivation did not result in increased pupation success except for larvae weighing > 0.14 g. Larvae responded to food deprivation by initiating and undergoing the same sequence of developmental events, requiring the same amount of time, as ad libitum‐fed larvae once those had reached their natural peak weight. Our results reveal a striking degree of flexibility in the dynamics and timing of larval development in O. taurus. They also suggest that premature exhaustion of a larva's food supply can serve as a cue for the initiation of metamorphosis. Premature metamorphosis in response to food deprivation has been documented in amphibians, but this is, to the best of our knowledge, the first time such a behaviour has been documented for a holometabolous insect. We discuss our findings in the context of the natural history and behavioural ecology of onthophagine beetles.

Olive Floral Bud Growth and Starch Content During Winter Rest and Spring Budbreak

In the olive (Olea europaea L.), inflorescence and flower differentiation occur in the early spring following a period of winter chilling and dormancy of the potentially reproductive buds. We examined the size, structure, and starch content of these buds during winter rest in the field and during forcing under standard growth-chamber conditions. Basic bud structure and dimensions remained unchanged during the rest period, but starch content increased in the bud's central axis. When cuttings were forced in the growth chamber, the buds followed a morphogenetic pattern similar to that observed in the field, but the sequence of developmental events could be timed more precisely. The first changes observed were the onset of axis growth and the differentiation of axillary primordia within 3 days of transfer to the growth chamber. This was followed by the initiation of new nodes, and, at 15 to 18 days, by the first signs of floral differentiation in the terminal and axillary bud apical meristems. Bud growth and differentiation were accompanied by a decrease in starch content.

Surviving Drosophila eye development: integrating cell death with differentiation during formation of a neural structure.

Normal differentiation requires an appropriately orchestrated sequence of developmental events. Regulation of cell survival and cell death is integrated with these events to achieve proper cell number, cell type, and tissue structure. Here we review regulation of cell survival in the context of a precisely patterned neural structure: the Drosophila compound eye. Numerous mutations lead to altered differentiation and are frequently accompanied by altered patterns of cell death. We discuss various critical times of normal eye development, highlighting how inappropriate regulation of cell death contributes to different mutant phenotypes associated with genes that specify the entire eye primordia, others that pattern the retina, and those that eliminate extraneous cells to refine the precise pigment cell lattice. Finally, we address how the Drosophila eye may allow identification of additional mechanisms that contribute to the normal integration of cell survival with appropriate events of cellular differentiation.

Expression of nitric oxide synthase in the developing rat hippocampus

Nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry was used to study the development of neurons synthesizing nitric oxide (NO) in the postnatal rat hippocampus. We show that NADPH-d reactive somata and processes are present from the day of birth until adulthood in the Ammon's horn. The dentate gyrus, however, has a more delayed period of nitric oxide synthase (NOS) expression with the staining appearing only by the end of the first postnatal week. Our results suggest that the time course of NOS expression correlates with the developmental sequence of events described in the hippocampus and that NO could be involved in the development of connections in this structure.

Developmental phenotypic plasticity: Where internalprogramming meets the external environment

Developmental plasticity has long been the focus of researchin both evolutionary ecology and molecular genetics. Recently, the concept of ontogenetic contingency has been proposed to indicate the dependence of plastic responses on the timing and sequence of developmental events. Also, the idea of the developmental reaction norm has been put forward to indicate the complex interactions among development, phenotypic plasticity, and allometry of different structures. Finally, for the first time, studies ranging from the ecological to the molecular aspects of the same plastic response are available on insect and flowering plant model systems.

In vitro studies on developmental morphology of Indian Podostemaceae

The early developmental biology of seven species of Indian podostemads based on in vitro growth of plants from seeds is discussed. Unpublished observations on seed germination, destiny of the radicular pole of the embryo, origin of the ‘primary axis’, location of the site of initiation of the thallus, and variations in seedling morphology in three thalloid members of the subfamily Podostemoideae (Zeylanidium lichenoides (S. Kurz) Engler, Hydrobryopsis sessilis (Willis) Engl., Willisia selaginoides (Bedd.) Warming ex Willis) are communicated. Additional observations are added to previously published accounts of the seedling biology of the thalloid Cladopus hookerianus (Tul.) C. Cusset and Polypleurum stylosum (Wight) Hall (Podostemoideae) and one thalloid Tristichoideae (Dalzellia ceylanica (Gardn.) Wight).Special attention is focused on the sequence of developmental events from seed to flowering in Indotristicha ramosissima (Wight) Van Royen (Tristichoideae), the only Indian species that seems to correspond to the Classical Root Shoot (CRS) model. In I. ramosissima exogenous root primordia arise from the flattened radicle, of which only three develop into main roots with asymmetric root caps. Although the mature seed lacks a plumule, a ‘primary axis’ of limited growth is formed at the apex. The plant body, with its numerous long branches, develops from the main roots. Flowering has been stimulated by subjecting vegetative plants to water and nutrient stress.Comparisons are made of early seedling developmental patterns among the seven investigated species. Special attention is focused on determining at what stage in ontogeny the root-shoot versus thalloid growth forms diverge. A model of seedling development is presented that depicts interspecific variability among species examined. The homology of the thallus in Podostemaceae remains unclear.