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Cell Death and Differentiation Mar 2019Autophagy-dependent cell death can be defined as cell demise that has a strict requirement of autophagy. Although autophagy often accompanies cell death following many... (Review)
Review
Autophagy-dependent cell death can be defined as cell demise that has a strict requirement of autophagy. Although autophagy often accompanies cell death following many toxic insults, the requirement of autophagic machinery for cell death execution, as established through specific genetic or chemical inhibition of the process, is highly contextual. During animal development, perhaps the best validated model of autophagy-dependent cell death is the degradation of the larval midgut during larval-pupal metamorphosis, where a number of key autophagy genes are required for the removal of the tissues. Surprisingly though, even in the midgut, not all of the 'canonical' autophagic machinery appears to be required. In other organisms and cancer cells many variations of autophagy-dependent cell death are apparent, pointing to the lack of a unifying cell death pathway. It is thus possible that components of the autophagy machinery are selectively utilised or repurposed for this type of cell death. In this review, we discuss examples of cell death that utilise autophagy machinery (or part thereof), the current knowledge of the complexity of autophagy-dependent cellular demise and the potential mechanisms and regulatory pathways involved in such cell death.
Topics: Animals; Apoptosis; Autophagic Cell Death; Autophagy; Drosophila; Humans; Metamorphosis, Biological; Signal Transduction
PubMed: 30568239
DOI: 10.1038/s41418-018-0252-y -
ELife Jul 2023Analysis of specimens preserved in amber from the Cretaceous period suggests that nematodes changed their host preference towards insects with a complete metamorphosis...
Analysis of specimens preserved in amber from the Cretaceous period suggests that nematodes changed their host preference towards insects with a complete metamorphosis more recently.
Topics: Animals; Fossils; Insecta; Nematoda; Amber; Metamorphosis, Biological
PubMed: 37449733
DOI: 10.7554/eLife.90008 -
Philosophical Transactions of the Royal... Oct 2019Metamorphosis and, in particular, holometaboly, the development of organisms through a series of discrete stages (egg, larva, pupa, adult) that hardly resemble one... (Review)
Review
Metamorphosis and, in particular, holometaboly, the development of organisms through a series of discrete stages (egg, larva, pupa, adult) that hardly resemble one another but are finely adapted to specific roles in the life cycle of the organism, has fascinated and mystified humans throughout history. However, it can be difficult to visualize the dramatic changes that occur during holometaboly without destructive sampling, traditionally through histology. However, advances in imaging technologies developed mainly for medical sciences have been applied to studies of insect metamorphosis over the past couple of decades. These include micro-computed tomography, magnetic resonance imaging and optical coherence tomography. A major advantage of these techniques is that they are rapid and non-destructive, enabling virtual dissection of an organism in any plane by anyone who has access to the image files and the necessary software. They can also be applied in some cases to visualize metamorphosis in vivo, including the periods of most rapid and dramatic morphological change. This review focusses on visualizing the intra-puparial holometabolous metamorphosis of cyclorraphous flies (Diptera), including the primary model organism for all genetic investigations, Drosophila melanogaster, and the blow flies of medical, veterinary and forensic importance, but also discusses similar studies on other insect orders. This article is part of the theme issue 'The evolution of complete metamorphosis'.
Topics: Animals; Diagnostic Imaging; Diptera; Drosophila melanogaster; Insecta; Larva; Metamorphosis, Biological; Pupa
PubMed: 31438819
DOI: 10.1098/rstb.2019.0071 -
Philosophical Transactions of the Royal... Oct 2019The majority of described hexapod species are holometabolous insects, undergoing an extreme form of metamorphosis with an intercalated pupal stage between the larva and... (Review)
Review
The majority of described hexapod species are holometabolous insects, undergoing an extreme form of metamorphosis with an intercalated pupal stage between the larva and adult, in which organs and tissues are extensively remodelled and in some cases completely rebuilt. Here, we review how and why this developmental strategy has evolved. While there are many theories explaining the evolution of metamorphosis, many of which fit under the hypothesis of decoupling of life stages, there are few clear adaptive hypotheses on why complete metamorphosis evolved. We propose that the main adaptive benefit of complete metamorphosis is decoupling between growth and differentiation. This facilitates the exploitation of ephemeral resources and enhances the probability of the metamorphic transition escaping developmental size thresholds. The evolution of complete metamorphosis comes at the cost of exposure to predators, parasites and pathogens during pupal life and requires specific adaptations of the immune system at this time. Moreover, metamorphosis poses a challenge for the maintenance of symbionts and the gut microbiota, although it may also offer the benefit of allowing an extensive change in microbiota between the larval and adult stages. The regulation of metamorphosis by two main players, ecdysone and juvenile hormone, and the related signalling cascades are now relatively well understood. The mechanics of metamorphosis have recently been studied in detail because of the advent of micro-CT and research into the role of cell death in remodelling tissues and organs. We support the argument that the adult stage must necessarily have preceded the larval form of the insect. We do not resolve the still contentious question of whether the larva of insects in general originated through the modification of existing preadult forms or through heterochrony as a modified embryonic stage (pronymph), nor whether the holometabolous pupa arose as a modified hemimetabolous final stage larva. This article is part of the theme issue 'The evolution of complete metamorphosis'.
Topics: Animals; Biological Evolution; Insecta; Metamorphosis, Biological
PubMed: 31438816
DOI: 10.1098/rstb.2019.0063 -
Developmental Dynamics : An Official... Jun 2021Amphibians display very diverse life cycles and development can be direct, where it occurs in ovo and a juvenile hatches directly, or biphasic, where an aquatic larva...
Amphibians display very diverse life cycles and development can be direct, where it occurs in ovo and a juvenile hatches directly, or biphasic, where an aquatic larva hatches and later undergoes metamorphosis followed by sexual maturation. In both cases, metamorphosis, corresponds to the post embryonic transition (PETr). A third strategy, only found in Urodeles, is more complex as larvae reach sexual maturity before metamorphosis, which can become accessory. The resulting paedomorphs retain their larval characters and keep their aquatic habitat. Does it mean that paedomorphs do not undergo PETr? Recent work using high throughput technologies coupled to system biology and developmental endocrinology revisited this question and provided novel datasets indicating that a paedomorph's "larval" tissue undergoes a proper developmental transition. Together with historical data, we propose that this transition is a marker of the PETr, which would be distinct from metamorphosis. This implies that (a) complex life cycles would result from the uncoupling of PETr and metamorphosis, and (b) biphasic life cycles would be a special cases where they occur simultaneously.
Topics: Amphibians; Animals; Larva; Life Cycle Stages; Metamorphosis, Biological
PubMed: 33527613
DOI: 10.1002/dvdy.304 -
Cells May 2022In multicellular organisms, development is based in part on the integration of communication systems. Two neuroendocrine axes, the hypothalamic-pituitary-thyroid and the... (Review)
Review
In multicellular organisms, development is based in part on the integration of communication systems. Two neuroendocrine axes, the hypothalamic-pituitary-thyroid and the hypothalamic-pituitary-adrenal/interrenal axes, are central players in orchestrating body morphogenesis. In all vertebrates, the hypothalamic-pituitary-thyroid axis controls thyroid hormone production and release, whereas the hypothalamic-pituitary-adrenal/interrenal axis regulates the production and release of corticosteroids. One of the most salient effects of thyroid hormones and corticosteroids in post-embryonic developmental processes is their critical role in metamorphosis in anuran amphibians. Metamorphosis involves modifications to the morphological and biochemical characteristics of all larval tissues to enable the transition from one life stage to the next life stage that coincides with an ecological niche switch. This transition in amphibians is an example of a widespread phenomenon among vertebrates, where thyroid hormones and corticosteroids coordinate a post-embryonic developmental transition. The review addresses the functions and interactions of thyroid hormone and corticosteroid signaling in amphibian development (metamorphosis) as well as the developmental roles of these two pathways in vertebrate evolution.
Topics: Adrenal Cortex Hormones; Amphibians; Animals; Metamorphosis, Biological; Thyroid Gland; Thyroid Hormones; Vertebrates
PubMed: 35626631
DOI: 10.3390/cells11101595 -
Cell Death and Differentiation Jan 2020The removal of superfluous and unwanted cells is a critical part of animal development. In insects the steroid hormone ecdysone, the focus of this review, is an... (Review)
Review
The removal of superfluous and unwanted cells is a critical part of animal development. In insects the steroid hormone ecdysone, the focus of this review, is an essential regulator of developmental transitions, including molting and metamorphosis. Like other steroid hormones, ecdysone works via nuclear hormone receptors to direct spatial and temporal regulation of gene transcription including genes required for cell death. During insect metamorphosis, pulses of ecdysone orchestrate the deletion of obsolete larval tissues, including the larval salivary glands and the midgut. In this review we discuss the molecular machinery and mechanisms of ecdysone-dependent cell and tissue removal, with a focus on studies in Drosophila and Lepidopteran insects.
Topics: Animals; Cell Death; Drosophila; Ecdysone; Lepidoptera; Metamorphosis, Biological; Molting
PubMed: 31745213
DOI: 10.1038/s41418-019-0456-9 -
Philosophical Transactions of the Royal... Oct 2019Many animals depend on microbial symbionts to provide nutrition, defence or other services. Holometabolous insects, as well as other animals that undergo metamorphosis,... (Review)
Review
Many animals depend on microbial symbionts to provide nutrition, defence or other services. Holometabolous insects, as well as other animals that undergo metamorphosis, face unique constraints on symbiont maintenance. Microbes present in larvae encounter a radical transformation of their habitat and may also need to withstand chemical and immunological challenges. Metamorphosis also provides an opportunity, in that symbiotic associations can be decoupled over development. For example, some holometabolous insects maintain the same symbiont as larvae and adults, but house it in different tissues; in other species, larvae and adults may harbour entirely different types or numbers of microbes, in accordance with shifts in host diet or habitat. Such flexibility may provide an advantage over hemimetabolous insects, in which selection on adult-stage microbial associations may be constrained by its negative effects on immature stages, and vice versa. Additionally, metamorphosis itself can be directly influenced by symbionts. Across disparate insect taxa, microbes protect hosts from pathogen infection, supply nutrients essential for rebuilding the adult body and provide cues regulating pupation. However, microbial associations remain completely unstudied for many families and even orders of Holometabola, and future research will undoubtedly reveal more links between metamorphosis and microbiota, two widespread features of animal life. This article is part of the theme issue 'The evolution of complete metamorphosis'.
Topics: Animals; Insecta; Larva; Metamorphosis, Biological; Microbiota; Symbiosis
PubMed: 31438811
DOI: 10.1098/rstb.2019.0068 -
Current Topics in Developmental Biology 2013Teleosts are the largest and most diverse group of vertebrates, and many species undergo morphological, physiological, and behavioral transitions, "metamorphoses," as... (Review)
Review
Teleosts are the largest and most diverse group of vertebrates, and many species undergo morphological, physiological, and behavioral transitions, "metamorphoses," as they progress between morphologically divergent life stages. The larval metamorphosis that generally occurs as teleosts mature from larva to juvenile involves the loss of embryo-specific features, the development of new adult features, major remodeling of different organ systems, and changes in physical proportions and overall phenotype. Yet, in contrast to anuran amphibians, for example, teleost metamorphosis can entail morphological change that is either sudden and profound, or relatively gradual and subtle. Here, we review the definition of metamorphosis in teleosts, the diversity of teleost metamorphic strategies and the transitions they involve, and what is known of their underlying endocrine and genetic bases. We suggest that teleost metamorphosis offers an outstanding opportunity for integrating our understanding of endocrine mechanisms, cellular processes of morphogenesis and differentiation, and the evolution of diverse morphologies and life histories.
Topics: Animals; Biodiversity; Endocrine System; Fishes; Metamorphosis, Biological; Morphogenesis
PubMed: 23347518
DOI: 10.1016/B978-0-12-385979-2.00005-8 -
ELife Mar 2023The way neurons in the brain rewire in larvae as they turn to adult fruit flies sheds light on how complete metamorphosis was 'invented' over the course of evolution.
The way neurons in the brain rewire in larvae as they turn to adult fruit flies sheds light on how complete metamorphosis was 'invented' over the course of evolution.
Topics: Animals; Brain; Arthropods; Fruit; Larva; Metamorphosis, Biological
PubMed: 36867155
DOI: 10.7554/eLife.86696