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ELife Jan 2023Mushroom bodies (MB) of adult have a core of thousands of Kenyon neurons; axons of the early-born g class form a medial lobe and those from later-born α'β' and αβ...
Mushroom bodies (MB) of adult have a core of thousands of Kenyon neurons; axons of the early-born g class form a medial lobe and those from later-born α'β' and αβ classes form both medial and vertical lobes. The larva, however, hatches with only γ neurons and forms a vertical lobe 'facsimile' using larval-specific axon branches from its γ neurons. MB input (MBINs) and output (MBONs) neurons divide the Kenyon neuron lobes into discrete computational compartments. The larva has 10 such compartments while the adult has 16. We determined the fates of 28 of the 32 MBONs and MBINs that define the 10 larval compartments. Seven compartments are subsequently incorporated into the adult MB; four of their MBINs die, while 12 MBINs/MBONs remodel to function in adult compartments. The remaining three compartments are larval specific. At metamorphosis their MBIN/MBONs trans-differentiate, leaving the MB for other adult brain circuits. The adult vertical lobes are made using MBONs/MBINs recruited from pools of adult-specific neurons. The combination of cell death, compartment shifting, trans-differentiation, and recruitment of new neurons result in no larval MBIN-MBON connections being maintained through metamorphosis. At this simple level, then, we find no anatomical substrate for a memory trace persisting from larva to adult. The adult phenotype of the trans-differentiating neurons represents their evolutionarily ancestral phenotype while their larval phenotype is a derived adaptation for the larval stage. These cells arise primarily within lineages that also produce permanent MBINs and MBONs, suggesting that larval specifying factors may allow information related to birth-order or sibling identity to be interpreted in a modified manner in the larva to allow these neurons to acquire larval phenotypic modifications. The loss of such factors at metamorphosis then allows these neurons to revert to their ancestral functions in the adult.
Topics: Animals; Drosophila; Larva; Neurons; Brain; Axons; Mushroom Bodies; Drosophila melanogaster; Metamorphosis, Biological
PubMed: 36695420
DOI: 10.7554/eLife.80594 -
Developmental Dynamics : An Official... Dec 2021Metamorphosis in marine species is characterized by profound changes at the ecophysiological, morphological, and cellular levels. The cnidarian Clytia hemisphaerica...
BACKGROUND
Metamorphosis in marine species is characterized by profound changes at the ecophysiological, morphological, and cellular levels. The cnidarian Clytia hemisphaerica exhibits a triphasic life cycle that includes a planula larva, a colonial polyp, and a sexually reproductive medusa. Most studies so far have focused on the embryogenesis of this species, whereas its metamorphosis has been only partially studied.
RESULTS
We investigated the main morphological changes of the planula larva of Clytia during the metamorphosis, and the associated cell proliferation and apoptosis. Based on our observations of planulae at successive times following artificial metamorphosis induction using GLWamide, we subdivided the Clytia's metamorphosis into a series of eight morphological stages occurring during a pre-settlement phase (from metamorphosis induction to planula ready for settlement) and the post-settlement phase (from planula settlement to primary polyp). Drastic morphological changes prior to definitive adhesion to the substrate were accompanied by specific patterns of stem-cell proliferation as well as apoptosis in both ectoderm and endoderm. Further waves of apoptosis occurring once the larva has settled were associated with morphogenesis of the primary polyp.
CONCLUSION
Clytia larval metamorphosis is characterized by distinct patterns of apoptosis and cell proliferation during the pre-settlement phase and the settled planula-to-polyp transformation.
Topics: Animals; Apoptosis; Cell Polarity; Cell Proliferation; Hydrozoa; Larva; Life Cycle Stages; Metamorphosis, Biological; Stem Cells
PubMed: 34036636
DOI: 10.1002/dvdy.376 -
Environmental Science & Technology Dec 2023Metamorphosis is a critical process in the life cycle of most marine benthic invertebrates, determining their transition from plankton to benthos. It affects dispersal...
Metamorphosis is a critical process in the life cycle of most marine benthic invertebrates, determining their transition from plankton to benthos. It affects dispersal and settlement and therefore decisively influences the dynamics of marine invertebrate populations. An extended period of metamorphic competence is an adaptive feature of numerous invertebrate species that increases the likelihood of finding a habitat suitable for settlement and survival. We found that crude oil and residues of burnt oil rapidly induce metamorphosis in two different marine invertebrate larvae, a previously unknown sublethal effect of oil pollution. When exposed to environmentally realistic oil concentrations, up to 84% of tested echinoderm larvae responded by undergoing metamorphosis. Similarly, up to 87% of gastropod larvae metamorphosed in response to burnt oil residues. This study demonstrates that crude oil and its burned residues can act as metamorphic inducers in marine planktonic larvae, short-circuiting adaptive metamorphic delay. Future studies on molecular pathways and oil-bacteria-metamorphosis interactions are needed to fully understand the direct or indirect mechanisms of oil-induced metamorphosis in marine invertebrates. With 90% of chronic oiling occurring in coastal areas, this previously undescribed impact of crude oil on planktonic larvae may have global implications for marine invertebrate populations and biodiversity.
Topics: Animals; Petroleum; Invertebrates; Metamorphosis, Biological; Ecosystem; Life Cycle Stages; Larva
PubMed: 37963269
DOI: 10.1021/acs.est.3c05194 -
Proceedings. Biological Sciences Nov 2022The shape and relative size of an ocular lens affect the focal length of the eye, with consequences for visual acuity and sensitivity. Lenses are typically spherical in...
The shape and relative size of an ocular lens affect the focal length of the eye, with consequences for visual acuity and sensitivity. Lenses are typically spherical in aquatic animals with camera-type eyes and axially flattened in terrestrial species to facilitate vision in optical media with different refractive indices. Frogs and toads (Amphibia: Anura) are ecologically diverse, with many species shifting from aquatic to terrestrial ecologies during metamorphosis. We quantified lens shape and relative size using 179 micro X-ray computed tomography scans of 126 biphasic anuran species and tested for correlations with life stage, environmental transitions, adult habits and adult activity patterns. Across broad phylogenetic diversity, tadpole lenses are more spherical than those of adults. Biphasic species with aquatic larvae and terrestrial adults typically undergo ontogenetic changes in lens shape, whereas species that remain aquatic as adults tend to retain more spherical lenses after metamorphosis. Further, adult lens shape is influenced by adult habit; notably, fossorial adults tend to retain spherical lenses following metamorphosis. Finally, lens size relative to eye size is smaller in aquatic and semiaquatic species than other adult ecologies. Our study demonstrates how ecology shapes visual systems, and the power of non-invasive imaging of museum specimens for studying sensory evolution.
Topics: Animals; Phylogeny; Anura; Bufonidae; Metamorphosis, Biological; Ecology; Larva
PubMed: 36382525
DOI: 10.1098/rspb.2022.0767 -
Endocrinology Jan 2023
Topics: Animals; Corticosterone; Larva; Xenopus laevis; Metamorphosis, Biological
PubMed: 36624971
DOI: 10.1210/endocr/bqad002 -
Proceedings of the National Academy of... May 2022How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth, and reproduction is an enduring question in marine...
How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth, and reproduction is an enduring question in marine science. Biofilm-induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon, the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles (OMVs) and complexes of phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure–function approach with a strong ecological focus, the cells and OMVs produced by C. lytica were interrogated to determine the class of the inductive compounds. Here, we report that larvae of H. elegans are induced to metamorphose by lipopolysaccharide produced by C. lytica. The widespread prevalence of lipopolysaccharide and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates.
Topics: Animals; Bacteria; Biofilms; Invertebrates; Larva; Lipopolysaccharides; Metamorphosis, Biological
PubMed: 35467986
DOI: 10.1073/pnas.2200795119 -
Pharmacology, Biochemistry, and Behavior Aug 2019Fundamental signs of epigenetic effects are variations in the expression of genes or phenotypic traits among isogenic mates. Therefore, genetically identical animals are... (Review)
Review
Fundamental signs of epigenetic effects are variations in the expression of genes or phenotypic traits among isogenic mates. Therefore, genetically identical animals are in high demand for epigenetic research. There are many genetically identical animals, including natural parthenogens and inbred laboratory lineages or clones. However, most parthenogenetic animal taxa are very small in combined epigenetic and drug addiction research. Orconectes rusticus has a unique phylogenetic position, with 2-3 years of life span, which undergoes metamorphosis that creates developmental stages with distinctly different morphologies, unique lifestyles, and broad behavioral traits, even among isogenic mates reared in the same environment offer novel inroads for epigenetics studies. Moreover, the establishment of crayfish as a novel system for drug addiction with evidence of an automated, operant self-administration and conditioned-reward, withdrawal, reinstatement of the conditioned drug-induced reward sets the stage to investigate epigenetic mechanisms of drug addiction. We discuss behavioral, pharmacological and molecular findings from laboratory studies that document a broad spectrum of molecular and, behavioral evidence including potential hypotheses that can be tested with the crayfish model for epigenetic study in drug addiction research.
Topics: Animals; Astacoidea; Behavior, Animal; Chromatin Assembly and Disassembly; Environmental Exposure; Epigenesis, Genetic; Gene Expression; Histones; Metamorphosis, Biological; Models, Animal; Reward; Self Administration; Substance-Related Disorders
PubMed: 31202808
DOI: 10.1016/j.pbb.2019.06.003 -
Integrative and Comparative Biology Sep 2023Many anuran amphibians (frogs and toads) rely on aquatic habitats during their larval stage. The quality of this environment can significantly impact lifetime fitness... (Meta-Analysis)
Meta-Analysis
Many anuran amphibians (frogs and toads) rely on aquatic habitats during their larval stage. The quality of this environment can significantly impact lifetime fitness and population dynamics. Over 450 studies have been published on environmental impacts on anuran developmental plasticity, yet we lack a synthesis of these effects across different environments. We conducted a meta-analysis and used a comparative approach to understand whether developmental plasticity in response to different larval environments produces predictable changes in metamorphic phenotypes. We analyzed data from 124 studies spanning 80 anuran species and six larval environments and showed that intraspecific variation in mass at metamorphosis and the duration of the larval period is partly explained by the type of environment experienced during the larval period. Changes in larval environments tended to reduce mass at metamorphosis relative to control conditions, with the degree of change depending on the identity and severity of environmental change. Higher temperatures and lower water levels shortened the duration of the larval period, whereas less food and higher densities increased the duration of the larval period. Phylogenetic relationships among species were not associated with interspecific variation in mass at metamorphosis plasticity or duration of the larval period plasticity. Our results provide a foundation for future studies on developmental plasticity, especially in response to global changes. This study provides motivation for additional work that links developmental plasticity with fitness consequences within and across life stages, as well as how the outcomes described here are altered in compounding environments.
Topics: Animals; Larva; Phylogeny; Physical Conditioning, Animal; Metamorphosis, Biological; Anura
PubMed: 37279893
DOI: 10.1093/icb/icad059 -
Advances in Kidney Disease and Health Nov 2023
Topics: Humans; Kidney Diseases; Metamorphosis, Biological; Diet
PubMed: 37988040
DOI: 10.1053/j.akdh.2023.10.005 -
PloS One 2023Amphibian metamorphosis is controlled by thyroid hormone (TH), which binds TH receptors (TRs) to regulate gene expression programs that underlie morphogenesis. Gene...
Amphibian metamorphosis is controlled by thyroid hormone (TH), which binds TH receptors (TRs) to regulate gene expression programs that underlie morphogenesis. Gene expression screens using tissues from premetamorphic tadpoles treated with TH identified some TH target genes, but few studies have analyzed genome-wide changes in gene regulation during spontaneous metamorphosis. We analyzed RNA sequencing data at four developmental stages from the beginning to the end of spontaneous metamorphosis, conducted on the neuroendocrine centers of Xenopus tropicalis tadpole brain. We also conducted chromatin immunoprecipitation sequencing (ChIP-seq) for TRs, and we compared gene expression changes during metamorphosis with those induced by exogenous TH. The mRNA levels of 26% of protein coding genes changed during metamorphosis; about half were upregulated and half downregulated. Twenty four percent of genes whose mRNA levels changed during metamorphosis had TR ChIP-seq peaks. Genes involved with neural cell differentiation, cell physiology, synaptogenesis and cell-cell signaling were upregulated, while genes involved with cell cycle, protein synthesis, and neural stem/progenitor cell homeostasis were downregulated. There is a shift from building neural structures early in the metamorphic process, to the differentiation and maturation of neural cells and neural signaling pathways characteristic of the adult frog brain. Only half of the genes modulated by treatment of premetamorphic tadpoles with TH for 16 h changed expression during metamorphosis; these represented 33% of the genes whose mRNA levels changed during metamorphosis. Taken together, our results provide a foundation for understanding the molecular basis for metamorphosis of tadpole brain, and they highlight potential caveats for interpreting gene regulation changes in premetamorphic tadpoles induced by exogenous TH.
Topics: Animals; Xenopus; Brain; Gene Expression Regulation; Anura; Metamorphosis, Biological
PubMed: 37384728
DOI: 10.1371/journal.pone.0287858