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Yolk-deprived Caenorhabditis elegans secure brood size at the expense of competitive fitness.

ABSTRACT: Oviparous animals support reproduction via the incorporation of yolk as a nutrient source into the eggs. In Caenorhabditis elegans, however, yolk proteins seem dispensable for fecundity, despite constituting the vast majority of the embryonic protein pool and acting as carriers for nutrient-rich lipids. Here, we used yolk protein-deprived C. elegans mutants to gain insight into the traits that may yet be influenced by yolk rationing. We show that massive yolk provisioning confers a temporal advantage during embryogenesis, while also increasing early juvenile body size and promoting competitive fitness. Opposite to species that reduce egg production under yolk deprivation, our results indicate that C. elegans relies on yolk as a fail-safe to secure offspring survival, rather than to maintain offspring numbers.

SUBMITTER: Geens E

PROVIDER: S-EPMC10105328 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Yolk-deprived Caenorhabditis elegans secure brood size at the expense of competitive fitness.

Geens Ellen E Van de Walle Pieter P Caroti Francesca F Jelier Rob R Steuwe Christian C Schoofs Liliane L Temmerman Liesbet L

Life science alliance 20230414 6

Oviparous animals support reproduction via the incorporation of yolk as a nutrient source into the eggs. In Caenorhabditis elegans, however, yolk proteins seem dispensable for fecundity, despite constituting the vast majority of the embryonic protein pool and acting as carriers for nutrient-rich lipids. Here, we used yolk protein-deprived C. elegans mutants to gain insight into the traits that may yet be influenced by yolk rationing. We show that massive yolk provisioning confers a ...[more]

PMID: 37059473

Similar Datasets

Yolk-deprived Caenorhabditis elegans secure brood size at the expense of competitive fitness

Project description:Oviparous animals support reproduction via the incorporation of yolk as a nutrient source into the eggs. In Caenorhabditis elegans, however, yolk proteins seem dispensable for fecundity, despite constituting the vast majority of the embryonic protein pool and acting as carriers for nutrient-rich lipids. Here, we used yolk protein-deprived C. elegans mutants to gain insight into the traits that may yet be influenced by yolk rationing. We show that massive yolk provisioning confers a temporal advantage during embryogenesis, while also increasing early juvenile body size and promoting competitive fitness. Opposite to species that reduce egg production under yolk deprivation, our results indicate that C. elegans relies on yolk as a fail-safe to secure offspring survival, rather than to maintain offspring numbers.

2023-04-12 | PXD041110 | Pride

Bacterial Respiration and Growth Rates Affect the Feeding Preferences, Brood Size and Lifespan of Caenorhabditis elegans.

Project description:Bacteria serve as live food and nutrients for bacterial-feeding nematodes (BFNs) in soils, and influence nematodes behavior and physiology through their metabolism. Five bacterial taxa (Bacillus amyloliquefaciens JX1, Variovorax sp. JX14, Bacillus megaterium JX15, Pseudomonas fluorescens Y1 and Escherichia coli OP50) and the typical BFN Caenorhabditis elegans were selected to study the effects of bacterial respiration and growth rates on the feeding preferences, brood size and lifespan of nematodes. P. fluorescens Y1 and E. coli OP50 were found to be more active, with high respiration and rapid growth, whereas B. amyloliquefaciens JX1 and B. megaterium JX15 were inactive. The nematode C. elegans preferred active P. fluorescens Y1 and E. coli OP50 obviously. Furthermore, worms that fed on these two active bacteria produced more offspring but had shorter lifespan, while inactive and less preferred bacteria had increased nematodes lifespan and decreased the brood size. Based on these results, we propose that the bacterial activity may influence the behavior and life traits of C. elegans in the following ways: (1) active bacteria reproduce rapidly and emit high levels of CO2 attracting C. elegans; (2) these active bacteria use more resources in the nematodes' gut to sustain their survival and reproduction, thereby reducing the worm's lifespan; (3) inactive bacteria may provide less food for worms than active bacteria, thus increasing nematodes lifespan but decreasing their fertility. Nematodes generally require a balance between their preferred foods and beneficial foods, only preferred food may not be beneficial for nematodes.

| S-EPMC4519269 | biostudies-literature

Assessment of Caenorhabditis elegans Competitive Fitness in the Presence of a Bacterial Parasite.

Project description:Accurate measurements of an organism's fitness are crucial for measuring evolutionary change. Methods of fitness measurement are most accurate when incorporating an individual's survival and fecundity, as well as accounting for any ecological interactions or environmental effects experienced by the organism. Here, we describe a protocol for measuring the relative mean fitness of Caenorhabditis elegans populations, or strains, through an assay that accounts for individual survival, fecundity, and intraspecific competitive ability in the presence of a bacterial parasite. In this competitive fitness assay nematodes from a focal population or strain are mixed with a GFP-marked tester strain in equal proportions, the mixture of nematodes are then exposed to a parasite, and the relative competitive fitness of the focal strain is determined by measuring the change in the ratio of focal nematodes to GFP-marked nematodes after one generation. Specifically, this protocol can be implemented to measure changes in nematode host fitness after experimental evolution by determining the relative competitive fitness of evolved versus ancestral nematode populations.

| S-EPMC8328670 | biostudies-literature

Genotype-dependent lifespan effects in peptone deprived Caenorhabditis elegans.

Project description:Dietary restriction appears to act as a general non-genetic mechanism that can robustly prolong lifespan. There have however been reports in many systems of cases where restricted food intake either shortens, or does not affect, lifespan. Here we analyze lifespan and the effect of food restriction via deprived peptone levels on lifespan in wild isolates and introgression lines (ILs) of the nematode Caenorhabditis elegans. These analyses identify genetic variation in lifespan, in the effect of this variation in diet on lifespan and also in the likelihood of maternal, matricidal, hatching. Importantly, in the wild isolates and the ILs, we identify genotypes in which peptone deprivation mediated dietary restriction reduces lifespan. We also identify, in recombinant inbred lines, a locus that affects maternal hatching, a phenotype closely linked to dietary restriction in C. elegans. These results indicate that peptone deprivation mediated dietary restriction affects lifespan in C. elegans in a genotype-dependent manner, reducing lifespan in some genotypes. This may operate by a mechanism similar to dietary restriction.

| S-EPMC4634109 | biostudies-literature

Intestine-to-neuronal signaling alters risk-taking behaviors in food-deprived Caenorhabditis elegans.

Project description:Animals integrate changes in external and internal environments to generate behavior. While neural circuits detecting external cues have been mapped, less is known about how internal states like hunger are integrated into behavioral outputs. Here, we use the nematode C. elegans to examine how changes in internal nutritional status affect chemosensory behaviors. We show that acute food deprivation leads to a reversible decline in repellent, but not attractant, sensitivity. This behavioral change requires two conserved transcription factors MML-1 (MondoA) and HLH-30 (TFEB), both of which translocate from the intestinal nuclei to the cytoplasm during food deprivation. Next, we identify the insulin-like peptide INS-31 as a candidate ligand relaying food-status signals from the intestine to other tissues. Further, we show that neurons likely use the DAF-2 insulin receptor and AGE-1/PI-3 Kinase, but not DAF-16/FOXO to integrate these intestine-released peptides. Altogether, our study shows how internal food status signals are integrated by transcription factors and intestine-neuron signaling to generate flexible behaviors via the gut-brain axis.

| S-EPMC9070953 | biostudies-literature

Size scaling of nucleolus in Caenorhabditis elegans embryos.

Project description:Nucleolus is viewed as a plurifunctional center in the cell, tightly linked to ribosome biosynthesis. As a non-membranous structure, how the size of nucleolus is determined is a long outstanding question, and the possibility of "direct size scaling to the nucleus" was raised by genetic studies in fission yeast. Here, we used the model organism Caenorhabditis elegans to test this hypothesis in multi-cellular organisms. We depleted ani-2, ima-3, or C27D9.1 by RNAi feeding, which altered embryo sizes to different extents in ncl-1 mutant worms. DIC imaging provided evidence that in size-altering embryo nucleolar size decreases in small cells and increases in large cells. Furthermore, analyses of nucleolar size in four blastomeres (ABa, ABp, EMS, and P2) within the same embryo of ncl-1 mutants consistently demonstrated the correspondence between cell and nucleolar sizes - the small cells (EMS and P2) have smaller nucleoli in comparison to the large cells (ABa).

| S-EPMC6306298 | biostudies-literature

A size threshold governs Caenorhabditis elegans developmental progression.

Project description:The growth of organisms from humans to bacteria is affected by environmental conditions. However, mechanisms governing growth and size control are not well understood, particularly in the context of changes in food availability in developing multicellular organisms. Here, we use a novel microfluidic platform to study the impact of diet on the growth and development of the nematode Caenorhabditis elegans. This device allows us to observe individual worms throughout larval development, quantify their growth as well as pinpoint the moulting transitions marking successive developmental stages. Under conditions of low food availability, worms grow very slowly, but do not moult until they have achieved a threshold size. The time spent in larval stages can be extended by over an order of magnitude, in agreement with a simple threshold size model. Thus, a critical worm size appears to trigger developmental progression, and may contribute to prolonged lifespan under dietary restriction.

| S-EPMC4632629 | biostudies-literature

Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?

Project description:BackgroundA central premise of physiological ecology is that an animal's preferred body temperature should correspond closely with the temperature maximizing performance and Darwinian fitness. Testing this co-adaptational hypothesis has been problematic for several reasons. First, reproductive fitness is the appropriate measure, but is difficult to measure in most animals. Second, no single fitness measure applies to all demographic situations, complicating interpretations. Here we test the co-adaptation hypothesis by studying an organism (Caenorhabditis elegans) in which both fitness and thermal preference can be reliably measured.ResultsWe find that natural isolates of C. elegans display a range of mean thermal preferences and also vary in their thermal sensitivities for fitness. Hot-seeking isolates CB4854 and CB4857 prefer temperatures that favor population growth rate (r), whereas the cold-seeking isolate CB4856 prefers temperatures that favor Lifetime Reproductive Success (LRS).ConclusionsCorrelations between fitness and thermal preference in natural isolates of C. elegans are driven primarily by isolate-specific differences in thermal preference. If these differences are the result of natural selection, then this suggests that the appropriate measure of fitness for use in evolutionary ecology studies might differ even within species, depending on the unique ecological and evolutionary history of each population.

| S-EPMC3141425 | biostudies-literature

Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans.

Project description:In the nematode Caenorhabditis elegans, loss of function of many genes leads to increases in lifespan, sometimes of a very large magnitude. Could this reflect the occurrence of programmed death that, like apoptosis of cells, promotes fitness? The notion that programmed death evolves as a mechanism to remove worn out, old individuals in order to increase food availability for kin is not supported by classic evolutionary theory for most species. However, it may apply in organisms with colonies of closely related individuals such as C. elegans in which largely clonal populations subsist on spatially limited food patches. Here, we ask whether food competition between nonreproductive adults and their clonal progeny could favor programmed death by using an in silico model of C. elegans. Colony fitness was estimated as yield of dauer larva propagules from a limited food patch. Simulations showed that not only shorter lifespan but also shorter reproductive span and reduced adult feeding rate can increase colony fitness, potentially by reducing futile food consumption. Early adult death was particularly beneficial when adult food consumption rate was high. These results imply that programmed, adaptive death could promote colony fitness in C. elegans through a consumer sacrifice mechanism. Thus, C. elegans lifespan may be limited not by aging in the usual sense but rather by apoptosis-like programmed death.

| S-EPMC7253062 | biostudies-literature

A multi-domain snail metallothionein increases cadmium resistance and fitness in Caenorhabditis elegans.

Project description:Metallothioneins (MTs) are a family of mostly low-molecular weight, cysteine-rich proteins capable of specific metal-ion binding that are involved in metal detoxification and homeostasis, as well as in stress response. In contrast to most other animal species which possess two-domain (bidominial) MTs, some gastropod species have evolved Cd2+-selective multidomain MTs (md-MTs) consisting of several concatenated β3 domains and a single C-terminal β1 domain. Each domain contains three-metal ion clusters and binds three metal ions. The terrestrial snail Alinda biplicata possesses, among other MT isoforms, an md-MT with nine β3 domains and a C-terminal β1 domain (termed 10md-MT), capable of binding up to 30 Cd2+ ions per protein molecule. In the present study, the Alinda biplicata 10md-MT gene and a truncated version consisting of one β3 domain and a single C-terminal β1 domain (2d-MT) were introduced into a Caenorhabditis elegans knock-out strain lacking a native MT gene (mtl-1). The two snail MT constructs consistently increased Cd2+ resistance, and partially improved morphological, life history and physiological fitness traits in the nematode model host Caenorhabditis elegans. This highlights how the engineering of transgenic Caenorhabditis elegans strains expressing snail MTs provides an enhancement of the innate metal detoxification mechanism and in doing so provides a platform for enhanced mechanistic toxicology.

| S-EPMC11513058 | biostudies-literature