Changes In Developmental Timing Research Articles

New hypotheses of cell type diversity and novelty from orthology-driven comparative single cell and nuclei transcriptomics in echinoderms.

Cell types are the building blocks of metazoan biodiversity and offer a powerful perspective for inferring evolutionary phenomena. With the development of single-cell transcriptomic techniques, new definitions of cell types are emerging. This allows a conceptual reassessment of traditional definitions of novel cell types and their evolution. Research in echinoderms, particularly sea star and sea urchin embryos has contributed significantly to understanding the evolution of novel cell types, through the examination of skeletogenic mesenchyme and pigment cells, which are found in sea urchin larvae, but not sea star larvae. This paper outlines the development of a gene expression atlas for the bat sea star, Patiria miniata, using single nuclear RNA sequencing (snRNA-seq) of embryonic stages. The atlas revealed 23 cell clusters covering all expected cell types from the endoderm, mesoderm, and ectoderm germ layers. In particular, four distinct neural clusters, an immune-like cluster, and distinct right and left coelom clusters were revealed as distinct cell states. A comparison with Strongylocentrotus purpuratus embryo single-cell transcriptomes was performed using 1:1 orthologs to anchor and then compare gene expression patterns. The equivalent of S. purpuratus piwil3+ Cells were not detected in P. miniata, while the Left Coelom of P. miniata has no equivalent cell cluster in S. purpuratus. These differences may reflect changes in developmental timing between these species. While considered novel morphologically, the Pigment Cells of S. purpuratus map to clusters containing Immune-like Mesenchyme and Neural cells of P. miniata, while the Skeletogenic Mesenchyme of S. purpuratus are revealed as orthologous to the Right Coelom cluster of P. miniata. These results suggest a new interpretation of the evolution of these well-studied cell types and a reflection on the definition of novel cell types.

Evolutionary mechanisms modulating the mammalian skull development.

Mammals possess impressive craniofacial variation that mirrors their adaptation to diverse ecological niches, feeding behaviour, physiology and overall lifestyle. The spectrum of craniofacial geometries is established mainly during embryonic development. The formation of the head represents a sequence of events regulated on genomic, molecular, cellular and tissue level, with each step taking place under tight spatio-temporal control. Even minor variations in timing, position or concentration of the molecular drivers and the resulting events can affect the final shape, size and position of the skeletal elements and the geometry of the head. Our knowledge of craniofacial development increased substantially in the last decades, mainly due to research using conventional vertebrate model organisms. However, how developmental differences in head formation arise specifically within mammals remains largely unexplored. This review highlights three evolutionary mechanisms acknowledged to modify ontogenesis: heterochrony, heterotopy and heterometry. We present recent research that links changes in developmental timing, spatial organization or gene expression levels to the acquisition of species-specific skull morphologies. We highlight how these evolutionary modifications occur on the level of the genes, molecules and cellular processes, and alter conserved developmental programmes to generate a broad spectrum of skull shapes characteristic of the class Mammalia. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

An atlas of the developing Tribolium castaneum brain reveals conservation in anatomy and divergence in timing to Drosophila melanogaster.

Insect brains are formed by conserved sets of neural lineages whose fibers form cohesive bundles with characteristic projection patterns. Within the brain neuropil, these bundles establish a system of fascicles constituting the macrocircuitry of the brain. The overall architecture of the neuropils and the macrocircuitry appear to be conserved. However, variation is observed, for example, in size, shape, and timing of development. Unfortunately, the developmental and genetic basis of this variation is poorly understood, although the rise of new genetically tractable model organisms such as the red flour beetle Tribolium castaneum allows the possibility to gain mechanistic insights. To facilitate such work, we present an atlas of the developing brain of T. castaneum, covering the first larval instar, the prepupal stage, and the adult, by combining wholemount immunohistochemical labeling of fiber bundles (acetylated tubulin) and neuropils (synapsin) with digital 3D reconstruction using the TrakEM2 software package. Upon comparing this anatomical dataset with the published work in Drosophila melanogaster, we confirm an overall high degree of conservation. Fiber tracts and neuropil fascicles, which can be visualized by global neuronal antibodies like antiacetylated tubulin in all invertebrate brains, create a rich anatomical framework to which individual neurons or other regions of interest can be referred to. The framework of a largely conserved pattern allowed us to describe differences between the two species with respect to parameters such as timing of neuron proliferation and maturation. These features likely reflect adaptive changes in developmental timing that govern the change from larval to adult brain.

SPASOS 1.1: a program for the inference of ancestral shape ontogenies.

We recently published a method to infer ancestral landmark-based shape ontogenies that takes into account the possible existence of changes in developmental timing. Here we describe SPASOS, a software to perform that analysis. SPASOS is an open-source Windows program written in C. Input data include landmark coordinates for each specimen -with the corresponding information about developmental timing- and a phylogenetic tree showing the relationships among the species sampled. As output, the program produces image files for an easy visualization of the results and data files useful for post-processing. The program incorporates an interpolating function, based on weighting moving averages, which allows analysis of data with scarce information along the ontogenetic trajectory. An empirical evaluation of this function showed its suitability to fill in incomplete ontogenetic trajectories. Finally, we present the results of a reanalysis in SPASOS of a published dataset, where changes in developmental timing were originally inferred by considering PCA scores as shape variables. Both approaches retrieved the same four largest changes in developmental timing, but differed in the ancestral shapes inferred.

PASOS: a method for the phylogenetic analysis of shape ontogenies.

We present a novel phylogenetic approach to infer ancestral ontogenies of shape characters described as landmark configurations. The method is rooted in previously published theoretical developments to analyse landmark data in a phylogenetic context with parsimony as the optimality criterion, in this case using the minimization of differences in landmark position to define not only ancestral shapes but also the changes in developmental timing between ancestor-descendant shape ontogenies. Evolutionary changes along the tree represent changes in relative developmental timing between ontogenetic trajectories (possible heterochronic events) and changes in shape within each stage. The method requires the user to determine the shape of the specimens between two standard events, for instance birth and onset of sexual maturity. Once the ontogenetic trajectory is discretized into a series of consecutive stages, the method enables the user to identify changes in developmental timing associated with changes in the offset and/or onset of the shape ontogenetic trajectories. The method is implemented in a C language program called SPASOS. The analysis of two empirical examples (anurans and felids) using this novel method yielded results in agreement with previous hypotheses about shape evolution in these groups based on non-phylogenetic analyses.

Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata

Diapause, an alternative developmental pathway characterized by changes in developmental timing and metabolism, is coordinated by molecular mechanisms that are not completely understood. MicroRNA (miRNA) mediated gene silencing is emerging as a key component of animal development and may have a significant role in initiating, maintaining, and terminating insect diapause. In the present study, we test this possibility by using high-throughput sequencing and qRT-PCR to discover diapause-related shifts in miRNA abundance in the flesh fly, Sarcophaga bullata. We identified ten evolutionarily conserved miRNAs that were differentially expressed in diapausing pupae compared to their nondiapausing counterparts. miR-289-5p and miR-1-3p were overexpressed in diapausing pupae and may be responsible for silencing expression of candidate genes during diapause. miR-9c-5p, miR-13b-3p, miR-31a-5p, miR-92b-3p, miR-275-3p, miR-276a-3p, miR-277-3p, and miR-305-5p were underexpressed in diapausing pupae and may contribute to increased expression of heat shock proteins and other factors necessary for the enhanced environmental stress-response that is a feature of diapause. In S. bullata, a maternal effect blocks the programming of diapause in progeny of females that have experienced pupal diapause, and in this study we report that several miRNAs, including miR-263a-5p, miR-100-5p, miR-125-5p, and let-7-5p were significantly overexpressed in such nondiapausing flies and may prevent entry into diapause. Together these miRNAs appear to be integral to the molecular processes that mediate entry into diapause.

Mammalian organogenesis in deep time: tools for teaching and outreach

Mammals constitute a rich subject of study on evolution and development and provide model organisms for experimental investigations. They can serve to illustrate how ontogeny and phylogeny can be studied together and how the reconstruction of ancestors of our own evolutionary lineage can be approached. Likewise, mammals can be used to promote 'tree thinking' and can provide an organismal appreciation of evolutionary changes. This subject is suitable for the classroom and to the public at large given the interest and familiarity of people with mammals and their closest relatives. We present a simple exercise in which embryonic development is presented as a transformative process that can be observed, compared, and analyzed. In addition, we provide and discuss a freely available animation on organogenesis and life history evolution in mammals. An evolutionary tree can be the best tool to order and understand those transformations for different species. A simple exercise introduces the subject of changes in developmental timing or heterochrony and its importance in evolution. The developmental perspective is relevant in teaching and outreach efforts for the understanding of evolutionary theory today.

Osteological Variation among Extreme Morphological Forms in the Mexican Salamander Genus Chiropterotriton (Amphibia: Plethodontidae): Morphological Evolution And Homoplasy.

Osteological variation is recorded among and within four of the most distinctive species of the Mexican salamander genus Chiropterotriton. Analysis of the data is consistent with the monophyletic status of the genus and documents previously unrecorded intraspecific and interspecific variation. Most of the recorded variation involves qualitative and quantitative proportional differences, but four fixed differences constitute autapomorphic states that affirm and diagnose some species (C. dimidiatus, C. magnipes). Osteological variation in 15 characters is analyzed with respect to predictions generated from four hypotheses: 1) phylogeny, 2) adaptation to specific habitats (the four species include cave-dwelling, terrestrial, and arboreal forms), 3) size-free shape, and 4) size. High levels of intraspecific variation suggest that the characters studied are not subject to rigid functional constraints in salamanders, regardless of size. The pattern predicted by the hypothesis based on size differences seen among these four Chiropterotriton species matches most closely the observed pattern of relative skull robustness. Since size change and heterochrony are often associated in plethodontid evolution, it is likely that changes in developmental timing play a role in the morphological transitions among these morphologically diverse taxa. Webbed feet, miniaturization, body shape, and an unusual tarsal arrangement are morphologies exhibited in species of Chiropterotrition that are shown to be homoplastic with other clades of tropical plethodontids. Although extensive homoplasy in salamanders might be seen as a roadblock to unraveling phylogenetic hypotheses, the homologous developmental systems that appear to underlie such homoplasy may reveal common and consistent evolutionary processes at work.

A meridic diet for continuous rearing of Arma chinensis (Hemiptera: Pentatomidae: Asopinae)

An artificial diet comprised of pig liver and tuna fish but devoid of insect components was developed for continuous rearing of the predator Arma chinensis Fallou. Our results demonstrated less desirable biological parameters in A. chinensis reared on this artificial diet compared to a secondary prey, pupae of Chinese oak silk moth Antheraea pernyi Guérin-Méneville. Weight of eggs and adults, fecundity and egg viability were lower for diet-fed A. chinensis compared to A. chinensis reared on pupae of A. pernyi. Developmental time from 2nd instar to adult and the preovipositional period were significantly longer for diet-fed A. chinensis. Cannibalism was also higher with diet-fed A. chinensis. Over successive generations of rearing on the diet some of the characteristics improved, such as developmental time, survival from 2nd instar to adult, sex ratio (♂:♀), adult weight, fecundity and fertility. These changes may indicate that the predators experience some degree of adaptation to, or genetic selection for, the diet after several consecutive generations. There were no changes in developmental time of egg and 1st instar, or survival from 1st to 2nd instar with successive generations reared on the artificial diet. However, diet-fed adults did live longer than pupae-fed adults.

A Comparison of the Sensory Development of Wolves (Canis lupus lupus) and Dogs (Canis lupus familiaris)

AbstractLittle is known about the development of the sensory systems of wolves. The timing of sensory development in wolves is usually extrapolated from studies on dogs, since they are members of the same species. However, early developmental differences between these two subspecies have already been identified. For example, wolves tend to approach and investigate objects in their environment 2 wk before dogs. These changes in developmental timing may play an important role in the behavioral differences between adult wolves and dogs. The purpose of this study is to compare the development of the sensory systems in wolves and dogs.Responses of seven wolf pups and 43 dog pups to familiar and novel olfactory, auditory, and visual stimuli were tested weekly from 2–7 wk of age. Eleven wolf pups were also observed for orientation towards auditory and visual stimuli during 2‐h sessions, 5 d a week, from 2–8 wk of age. These observations were supplemented by the daily records of caretakers.The results suggest that wolves and dogs both develop olfaction by 2 wk, audition by 4 wk, and vision by 6 wk on average, despite the 2‐wk shift in their ability to explore. This means that when wolves begin to explore at 2 wk, they are blind and deaf, and must rely primarily on their sense of smell. Thus, there is a significant alteration of how these subspecies experience their environment during the critical period of socialization. These findings lead to an alternative explanation for the difference in dogs' and wolves' abilities to form interspecies social attachments, such as those with humans.

Causes and consequences of expanded subventricular zones

Primates have evolved an expanded isocortex relative to many other mammals. Parrots and songbirds have evolved an expanded telencephalon relative to many other birds. Previous work suggests that the expansion of the telencephalon in parrots and songbirds as well as the isocortex in primates is achieved, at least in part, by selectively delaying neurogenesis, expanding the subventricular zone (SVZ) and delaying maturation. The finding that similar developmental alterations in the spatial and temporal pattern of neurogenesis evolved together in these two distant lineages suggests that a single change in developmental mechanism might account for the expansion of the isocortex or telencephalon. We here review how uniformly lengthening developmental schedules may result in delays of neurogenesis, the expansion of the SVZ and delayed maturation. We propose that delays in neurogenesis may cause ventricular zone (VZ) cells to proliferate faster than the VZ can expand, which may force many proliferating cells to leave the VZ and form an expanded SVZ. Prolonged proliferation in the VZ and SVZ causes delays in neuronal maturation, which in turn may promote learning from conspecifics. Thus, we suggest that a single heterochronic change in developmental timing may orchestrate a variety of changes in the spatial and temporal pattern of proliferation, which has important behavioral consequences in adulthood.

Gonad development in Midas cichlids and the evolution of sex change in fishes

Some fishes mature and function as one sex and later transform to the other sex in response to social interactions. Previous evidence suggested that a change in developmental timing may be involved in the evolution of adult sex change in fishes. The most recent support for this idea came from reports that sex in the Midas cichlid, Amphilophus citrinellus, was determined by social conditions experienced at the juvenile stage. Differentiation as a male was reported to be dependent on large body size relative to group-mates, and thought to be mediated through aggressive interactions. Here I demonstrate that socially controlled sex determination does not occur as was originally reported. Previously, I found that sex was not associated with body size in juveniles either in nature or in captivity. Similarly, I found no association between aggressive behavior and sex in juveniles. I later demonstrated that socially controlled sex determination does not typically occur in the Midas cichlid and closely related species and supported an alternative mechanism to explain large body size in adult males. Finally, in the current study I analyze gonad histology of fish from the same population used by the original authors and lay to rest the idea of socially controlled sex determination in this species. Recent observations of socially controlled sex determination in juveniles of species that typically change sex at the adult stage are examples of phenotypic plasticity, not genetic variation. Therefore, juvenile socially controlled sex determination does not support a theory that a change in developmental timing is involved in the evolution of adult sex change in fishes.

Epigenetic regulation of development links adaption and diversification of skeletal phenotypes: a case study in shrews

A major goal of evolutionary biology is to understand how diversity is generated. One hypothesis suggests that evolutionary change is facilitated by environmental sensitivity of development and the associated modifications of organismal development that induce selectable phenotypic variation. In vertebrates, growth and development of bones is partially guided by contractions of the attached musculature. During ontogeny, this muscle activity changes from sporadic motility to functional use. Thus, shifts in timing of ossification can either buffer development from environmental signals, or enable environmental signals to influence bone development and generate specialized skeletal adaptations. Here, we outline a conceptual framework for future studies that focuses on mediation of phenotypic plasticity in skeletal development through changes in developmental timing and provide evidence for the importance of developmental timing for adaptation and diversification in shrews.

Induced niche shift as an anti-predator response for an endoparasitoid

When two developmental stages do not share the same ecological niche, the control of the niche shift through a change in developmental timing, referred to as 'heterokairy', can provide an adaptive advantage for the individual (e.g. if mortality risk is higher in the first niche). For endoparasitic species that develop inside another (host) species, mortality of the host may directly induce mortality risk for the parasite. Thus, endoparasitoid larvae should be selected for response to host predation. In this study, aphids previously parasitized by the endoparasitoid Endaphis fugitiva, Gagné and Muratori (Diptera: Cecidomyiidae), were experimentally exposed to increased mortality risks. Both simulated attack and actual predator attacks against aphid hosts induced early emergence of the parasitoid larvae. Parasitoid emergence from the aphids occurred several minutes before the predator finished feeding on the aphid, allowing enough time for the parasitoid larvae to avoid direct predation. Predator-induced emergence produced significantly smaller parasitoid larvae than controls, but, interestingly, no effect on Endaphis adult size was found. To our knowledge, this is the first evidence of induced emergence in an insect parasitoid, but we suggest that this mechanism might be at work in many other species where plasticity in development time allows the individual to perform an adaptive niche shift.

Secondary Growth in Vertebraria Roots from the Late Permian of Antarctica: A Change in Developmental Timing

Permineralized Vertebraria roots from the late Permian of the Central Transantarctic Mountains, Antarctica, are investigated to understand the unusual vascular anatomy of the genus. The specimens range from ∼1 mm to several centimeters in diameter and illustrate all the stages of secondary growth. Our observations confirm previous hypotheses on the development of these roots and suggest that their unique anatomy is the result of a change in developmental timing. Vertebraria is characterized by a vascular cambium that remains discontinuous through several growth seasons, leading to the formation of lacunae alternating in cross section with wedges of secondary vascular tissues. The bifacial nature of the cambium is confirmed by the presence of well‐developed secondary phloem composed of longitudinally elongated cells and uniseriate parenchymatous rays. In some of the largest specimens, a continuous vascular cylinder is formed by the differentiation of cambium from parenchymatous cells bordering the lacunae....

Spectacular morphological novelty in a miniature cyprinid fish, Danionella dracula n. sp.

Danionella dracula is a new species of sexually dimorphic, miniature and highly developmentally truncated cyprinid fish. Compared with its close relative, the zebrafish Danio rerio, it lacks 44 bones or parts thereof and represents one of the most developmentally truncated vertebrates. Absence of the majority of bones appears to be due to developmental truncation via terminal deletion. In contrast to these larval-like features, D. dracula also shows several hyperossifications. Uniquely, among carp-like fishes, male D. dracula have a series of long, pointed odontoid processes on the jaws greatly resembling the jaw dentition of teleosts with true teeth. The anterior-most process in each jaw is extended as a canine-like fang projecting through the epithelium. True jaw teeth are absent from all 3700 species of cypriniforms and were lost at least in the Upper Eocene. It remains to be investigated, however, whether the conserved pathways to regulate tooth development in cypriniforms have been used in D. dracula to form and pattern the odontoid processes. This new species represents a remarkable example linking progenetic paedomorphosis via heterochronic change in developmental timing to the evolution of morphological novelties.

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.

A developmental perspective on evolutionary innovation in the radula of the predatory neogastropod family Muricidae*

The neogastropod family Muricidae includes a diverse set of radular bauplane, including a beaked, three-dimensional form, a flattened-pentacusped form, and a third “dagger” type in which the central rachidian cusp is massive and elongate. Examination of the radular ontogenies of representatives of five muricid subfamilies reveals that several species undergo changes in radular form during ontogeny on a scale comparable to the evolutionary differences between higher taxa. The species Concholepas concholepas (Bruguière, 1789) (Rapaninae) and Trophon geversianus (Pallas, 1774) (Trophoninae) begin ontogeny with a three-dimensional rachidian characteristic of the Ocenebrinae or Muricopsinae but end with the dagger rachidian typical of their respective subfamilies. Young individuals of Vitularia salebrosa (King and Broderip, 1832) (Muricopsinae?) also have a three-dimensional rachidian but shift to a double-dagger morphology by adulthood. Chicoreus (Phyllonotus) pomum (Gmelin, 1791) (Muricinae) has a typical flattened muricine rachidian as an adult but possesses a “buccinoid”-like rachidian just after hatching. Urosalpinx cinerea (Say, 1822) (Ocenebrinae), was unique among the species examined in exhibiting no ontogenetic changes in radular form. The occurrence of two radular bauplane within the same individual snail during ontogeny suggests great potential for rapid, convergent evolution of adult features through simple changes in developmental timing. A three-dimensional rachidian, for example, could be retained into adulthood through paedomorphosis in any lineage possessing the three-dimensional-to-dagger ontogeny. Systematic assignments of muricids based solely on radular features should be reexamined.

Forelimb-hindlimb developmental timing changes across tetrapod phylogeny

BackgroundTetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.ResultsAn overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.ConclusionMajor heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.

Language and life history: Not a new perspective

The uniqueness of human cognition and language has long been linked to systematic changes in developmental timing. Selection for postnatal skeletal ossification resulted in progressive prolongation of universal patterns of primate growth, lengthening infancy, childhood, and adolescence. Language emerged as communication increased in complexity within and between communities rather than from selection for some unique features of childhood or adolescence, or both.