Organismal Fitness Research Articles

Human culture is uniquely open-ended rather than uniquely cumulative.

Theories of how humans came to be so ecologically dominant increasingly centre on the adaptive abilities of human culture and its capacity for cumulative change and high-fidelity transmission. Here we revisit this hypothesis by comparing human culture with animal cultures and cases of epigenetic inheritance and parental effects. We first conclude that cumulative change and high transmission fidelity are not unique to human culture as previously thought, and so they are unlikely to explain its adaptive qualities. We then evaluate the evidence for seven alternative explanations: the inheritance of acquired characters, the pathways of inheritance, the non-random generation of variation, the scope of heritable variation, effects on organismal fitness, effects on genetic fitness and effects on evolutionary dynamics. From these, we identify the open-ended scope of human cultural variation as a key, but generally neglected, phenomenon. We end by articulating a hypothesis for the cognitive basis of this open-endedness.

Crossed effects of helminth infection and lead exposure on fitness: An experimental study in feral pigeons (Columba livia).

Living organisms are exposed to multiple environmental factors that can affect their fitness. The negative effects of these simultaneous stressors can be additive or can interact in negative synergistic or antagonistic ways to affect the health of exposed individuals. Parasites can accumulate pollutants in their own tissues and have been shown to increase the tolerance of their hosts to different pollutants (antagonistic interaction between parasites and pollutants). Through an experimental approach, we tested the existence of combined antagonistic effects between intestinal parasites and lead exposure on urban feral pigeons (Columba livia) which are known to be exposed to trace metal pollution and harbour a wide variety of internal and external parasites. We experimentally exposed wild feral pigeons in captivity to two treatments: an anthelmintic treatment to eliminate intestinal nematode parasites; an exposure to lead for a period of 6 months. We tested the effects of these crossed treatments on several components of fitness: immunocompetence, reproduction, and body mass. Our findings suggest that the overall effects of lead exposure, either alone or in combination with the presence of intestinal parasites (without anthelmintic treatment) were negative, through either additive or synergistic means. Our results reveal the existence of negative combined effects between pollutant exposure and intestinal parasites, highlighting the importance of accounting for multiple stress factors when studying the effects of exposure to pollutants and/or other environmental stressors on the fitness of organisms.

ASI-RIM neuronal axis regulates systemic mitochondrial stress response via TGF-β signaling cascade.

Morphogens play a critical role in coordinating stress adaptation and aging across tissues, yet their involvement in neuronal mitochondrial stress responses and systemic effects remains unclear. In this study, we reveal that the transforming growth factor beta (TGF-β) DAF-7 is pivotal in mediating the intestinal mitochondrial unfolded protein response (UPRmt) in Caenorhabditis elegans under neuronal mitochondrial stress. Two ASI sensory neurons produce DAF-7, which targets DAF-1/TGF-β receptors on RIM interneurons to orchestrate a systemic UPRmt response. Remarkably, inducing mitochondrial stress specifically in ASI neurons activates intestinal UPRmt, extends lifespan, enhances pathogen resistance, and reduces both brood size and body fat levels. Furthermore, dopamine positively regulates this UPRmt activation, while GABA acts as a systemic suppressor. This study uncovers the intricate mechanisms of systemic mitochondrial stress regulation, emphasizing the vital role of TGF-β in metabolic adaptations that are crucial for organismal fitness and aging during neuronal mitochondrial stress.

Reproductive response of the predator Tenuisvalvae notata (Mulsant) (Coleoptera: Coccinellidae) to temperatures outside their ideal thermal range.

Global warming has driven changes in the biology and fitness of organisms that need to adapt to temperatures outside of their optimal range to survive. This study investigated aspects of reproduction and survival of the lady beetle Tenuisvalvae notata (Mulsant) (Coleoptera: Coccinellidae) subjected to temperatures that varied from its optimal (28°C) to a gradual decrease (12, 14, 16, and 18°C) and increase (32, 34, 35, and 36°C) over time at a rate of 1°C/day. Fertility, fecundity, oviposition period, and survival were determined. There was a significant reduction in fertility and fecundity at temperatures below 18°C and above 34°C, whereas survival was reduced only above 34°C. Additionally, we evaluated that fecundity was the lowest when females were kept at low temperature, and when males were kept under high temperature. Therefore, if the T. notata remained for a long period under exposure to temperatures outside the ideal range, then the species could present different reproductive responses for each sex to high and low temperatures. This factor must be considered when releasing natural enemies into an area to understand the effect of temperature on the decline of a local population a few generations after release.

Impacts of graphene oxide contamination on a food web: Threats to somatic and reproductive health of organisms

Contamination of aquatic food webs with nanomaterials poses a significant ecological and human health challenge. Ingestion of nanomaterials alongside food disrupts digestion and impairs physiological processes, with potential consequences for organism fitness and survival. Complex interactions between nanomaterials and biota further exacerbate the issue, influencing life-history strategies and ecosystem dynamics. Accumulation of nanomaterials within autotrophic and detritus-based food webs raises concerns about biomagnification, especially for top-level consumers and seafood-dependent human populations. Understanding the extent and impact of nanomaterial contamination on aquatic biota is crucial for effective mitigation strategies. To address this challenge, we conducted a comprehensive study evaluating the bioaccumulation effects of graphene oxide (GO), a commonly used nanomaterial, within an aquatic food chain. Using a gnotobiotic freshwater microcosm, we investigated the effects of micro- and nano-scale GO sheets on key organisms: green algae (Chlorella vulgaris), brine shrimp (Artemia salina), and zebrafish (Danio rerio). Two feeding regimes, direct ingestion and trophic transfer, were employed to assess GO uptake and transfer within the food web. Direct exposure involved individual organisms being exposed to either nano- or micro-scale GO sheets, while trophic transfer involved a sequential exposure pathway: algae exposed to GO sheets, artemias feeding on the algae, and zebrafish consuming the artemias. Our study provides critical insights into nanomaterial contamination in aquatic ecosystems. Physicochemical properties of GO sheets, including ζ-potential and dispersion, were influenced by salt culture media, resulting in aggregation under salt conditions. Microscopic imaging confirmed the bioaccumulation of GO sheets within organisms, indicating prolonged exposure and potential long-term effects. Notably, biodistribution analysis in zebrafish demonstrated the penetration of nano-sized GO into the intestinal wall, signifying direct interaction with vital organs. Exposure to GO resulted in increased zebrafish mortality and impaired reproductive performance, particularly through trophic transfer. These findings emphasize the urgent need to address nanomaterial contamination in aquatic food webs to protect ecosystem components and human consumers. Our study highlights the importance of developing effective mitigation strategies to preserve the integrity of aquatic ecosystems, ensure resource sustainability, and safeguard human well-being. In conclusion, our study provides crucial insights into the impact of nanomaterial pollution on aquatic biota. By recognizing the challenges posed by nanomaterial contamination and implementing targeted interventions, we can mitigate the adverse effects, preserving the integrity of aquatic ecosystems and safeguarding human health.

Diurnal.plant.tools in 2024: expanding to Marchantia polymorpha and four angiosperms.

Diurnal gene expression is a pervasive phenomenon occurring across all kingdoms of life, orchestrating adaptive responses to daily environmental fluctuations and thus enhancing organismal fitness. Our understanding of the plant circadian clock is primarily derived from studies in Arabidopsis and direct comparisons are difficult due to differences in gene family sizes. To this end, the identification of functional orthologs based on diurnal and tissue expression is necessary. The diurnal.plant.tools database constitutes a repository of gene expression profiles from 17 members of the Archaeplastida lineage, with built-in tools facilitating cross-species comparisons. In this database update, we expand the dataset with diurnal gene expression from 4 agriculturally significant crop species and Marchantia, a plant of evolutionary significance. Notably, the inclusion of diurnal gene expression data for Marchantia enables researchers to glean insights into the evolutionary trajectories of the circadian clock and other biological processes spanning from algae to angiosperms. Moreover, integrating diurnal gene expression data with datasets from related gene co-expression databases, such as CoNekt-Plants and CoNekt-Stress, which contain gene expression data for tissue and perturbation experiments, provides a comprehensive overview of gene functions across diverse biological contexts. This expanded database serves as a valuable resource for elucidating the intricacies of diurnal gene regulation and its evolutionary underpinnings in plant biology.

Chromatic acclimation in cyanobacteria renders robust photosynthesis and fitness in dynamic light environment: Recent advances and future perspectives.

Cyanobacteria are photoautotrophic organisms that use light and water as a source of energy and electrons, respectively, to fix atmospheric carbon dioxide and release oxygen as a by-product during photosynthesis. However, photosynthesis and fitness of organisms are challenged by seasonal and diurnal fluctuations in light environments. Also, the distribution of cyanobacteria in a water column is subject to changes in the light regime. The quality and quantity of light change significantly in low and bright light environments that either limit photochemistry or result in photoinhibition due to an excess amount of light reaching reaction centers. Therefore, cyanobacteria have to adjust their light-harvesting machinery and cell morphology for the optimal harvesting of light. This adjustment of light-harvesting involves remodeling of the light-harvesting complex called phycobilisome or incorporation of chlorophyll molecules such as chlorophyll d and f into their light-harvesting machinery. Thus, photoacclimation responses of cyanobacteria at the level of pigment composition and cell morphology maximize their photosynthetic ability and fitness under a dynamic light environment. Cyanobacteria exhibit different types of photoacclimation responses that are commonly known as chromatic acclimation (CA). In this work, we discuss different types of CA reported in cyanobacteria and present a molecular mechanism of well-known type 3 CA where phycoerythrin and phycocyanin of phycobilisome changes according to light signals. We also include other aspects of type 3 CA that have been recently studied at a molecular level and highlight the importance of morphogenes, cytoskeleton, and carboxysome proteins. In summary, CA gives a unique competitive benefit to cyanobacteria by increasing their resource utilization ability and fitness.

Microbial DNA extraction method for avian feces and preen oil from diverse species.

As DNA sequencing technology continues to rapidly improve, studies investigating the microbial communities of host organisms (i.e., microbiota) are becoming not only more popular but also more financially accessible. Across many taxa, microbiomes can have important impacts on organismal health and fitness. To evaluate the microbial community composition of a particular microbiome, microbial DNA must be successfully extracted. Fecal samples are often easy to collect and are a good source of gut microbial DNA. Additionally, interest in the avian preen gland microbiome is rapidly growing, due to the importance of preen oil for many aspects of avian life. Microbial DNA extractions from avian fecal and preen oil samples present multiple challenges, however. Here, we describe a modified PrepMan Ultra Sample Preparation Reagent microbial DNA extraction method that is less expensive than other commonly used methodologies and is highly effective for both fecal and preen oil samples collected from a broad range of avian species. We expect our method will facilitate microbial DNA extractions from multiple avian microbiome reservoirs, which have previously proved difficult and expensive. Our method therefore increases the feasibility of future studies of avian host microbiomes.

Poly-alanine-tailing is a modifier of neurodegeneration caused by Listerin mutation.

The surveillance of translation is critical for the fitness of organisms from bacteria to humans. Ribosome-associated Quality Control (RQC) is a surveillance mechanism that promotes the elimination of truncated polypeptides, byproducts of ribosome stalling during translation. In canonical mammalian RQC, NEMF binds to the large ribosomal subunit and recruits the E3 ubiquitin ligase Listerin, which marks the nascent-chains for proteasomal degradation. NEMF additionally extends the nascent-chain's C-terminus with poly-alanine ('Ala-tail'), exposing lysines in the ribosomal exit tunnel for ubiquitination. In an alternative, Listerin-independent RQC pathway, released nascent-chains are targeted by Ala-tail-binding E3 ligases. While mutations in Listerin or in NEMF selectively elicit neurodegeneration in mice and humans, the physiological significance of Ala-tailing and its role in disease have remained unknown. Here, we report the analysis of mice in which NEMF's Ala-tailing activity was selectively impaired. Whereas the Nemf homozygous mutation did not affect lifespan and only led to mild motor defects, genetic interaction analyses uncovered its synthetic lethal phenotype when combined with the lister neurodegeneration-causing mutation. Conversely, the lister phenotype was markedly improved when Ala-tailing capacity was partially reduced by a heterozygous Nemf mutation. Providing a plausible mechanism for this striking switch from early neuroprotection to subsequent neurotoxicity, we found that RQC substrates that evade degradation form amyloid-like aggregates in an Ala-tail dependent fashion. These findings uncover a critical role for Ala-tailing in mammalian proteostasis, and deepen our molecular understanding of pathophysiological roles of RQC in neurodegeneration.

Analysis of subcellular energy metabolism in five Lacertidae lizards across varied environmental conditions

Aerobic respiration is the main energy source for most eukaryotes, and efficient mitochondrial energy transfer greatly influences organismal fitness. To survive environmental changes, cells have evolved to adjust their biochemistry. Thus, measuring energy metabolism at the subcellular level can enhance our understanding of individual performance, population dynamics, and species distribution ranges. We investigated three important metabolic traits at the subcellular level in five lacertid lizard species sampled from different elevations, from sea level up to 2000 m. We examined hemoglobin concentration, two markers of oxidative stress (catalase activity and carbonyl concentration) and maximum rate of metabolic respiration at the subcellular level (potential metabolic activity at the electron transport system). The traits were analysed in laboratory acclimated adult male lizards to investigate the adaptive metabolic responses to the variable environmental conditions at the local sampling sites. Potential metabolic activity at the cellular level was measured at four temperatures – 28 °C, 30 °C, 32 °C and 34 °C – covering the range of preferred body temperatures of the species studied. Hemoglobin content, carbonyl concentration and potential metabolic activity did not differ significantly among species. Interspecific differences were found in the catalase activity, Potential metabolic activity increased with temperature in parallel in all five species. The highest response of the metabolic rate with temperature (Q10) and Arrhenius activation energy (Ea) was recorded in the high-mountain species Iberolacerta monticola.

An autoregulatory poison exon in Smndc1 is conserved across kingdoms and influences organism growth.

Many of the most highly conserved elements in the human genome are "poison exons," alternatively spliced exons that contain premature termination codons and permit post-transcriptional regulation of mRNA abundance through induction of nonsense-mediated mRNA decay (NMD). Poison exons are widely assumed to be highly conserved due to their presumed importance for organismal fitness, but this functional importance has never been tested in the context of a whole organism. Here, we report that a poison exon in Smndc1 is conserved across mammals and plants and plays a molecular autoregulatory function in both kingdoms. We generated mouse and A. thaliana models lacking this poison exon to find its loss leads to deregulation of SMNDC1 protein levels, pervasive alterations in mRNA processing, and organismal size restriction. Together, these models demonstrate the importance of poison exons for both molecular and organismal phenotypes that likely explain their extraordinary conservation.

Effects of parental diet on Mormon cricket egg diapause, embryonic development rate, and periodic outbreaks

Transgenerational phenotypic modification can alter organismal fitness, population demographics, and community interactions. For ectotherms, both dietary composition and temperature have important effects on organismal fitness, but they are rarely investigated together. Mormon crickets Anabrus simplex are capable of diapausing as eggs in the soil for multiple years with duration largely dependent on cumulative heat units or degree days. Because Mormon crickets can be abundant in the landscape in one year and disappear suddenly the next, I asked: does parental nutrition affect the duration of egg diapause? Beginning in the ultimate nymphal instar, Mormon crickets were fed a diet high in protein, one equal in protein to carbohydrate, or a diet high in carbohydrates and the time for eggs to develop after they were laid was measured. If parental nutrition affects temperature-sensitive egg diapause, then that change in sensitivity to temperature might also alter the relationship between embryonic development rate and temperature. I asked: does parental nutrition affect embryonic development rate as a function of temperature? To this end, I manipulated densities of Mormon cricket nymphs and protein-rich prey (grasshoppers) in field cages, collected eggs from the adult Mormon crickets, and measured the optimal temperature, maximum development rate, and thermal breadth for embryonic development of the offspring. I found that Mormon crickets fed a high protein diet laid eggs with shorter diapause. Consistent with this long-term result, those housed with the most grasshoppers to eat laid eggs that had the fastest maximum development rate, whereas those without grasshoppers laid eggs with slower maximum developmental rates but the broadest thermal breadth. Eggs from Mormon crickets housed with intermediate levels of grasshopper densities had a decline in peak development rate with an increase in density. In addition, Mormon crickets housed with more conspecifics laid eggs with faster development rates, whereas thermal breadth and the temperature optima were not affected by cricket density. As predicted, Mormon cricket diets significantly affected egg diapause and development rates. Contrary to expectations based on observed changes in diet preferences during a Mormon cricket outbreak, Mormon crickets fed high protein diets laid eggs with significantly shorter egg diapause and significantly faster egg development rates. Interestingly, doubling of Mormon cricket density caused eggs to develop in nearly half the time. This latter result indicates that Mormon cricket aggregations promote rapid development of progeny. Moreover, the tight, linear structure of migratory bands in which females intermittently stop to lay eggs assures that the progeny hatch and develop in dense cohorts. In this manner, the banding behavior might carry-over into subsequent generations as long as cohorts are dense and protein is available. With band thinning or protein restriction, females spread their bet-hedging and progeny remain longer as eggs in the soil.

Pangenome reconstruction of Lactobacillaceae metabolism predicts species-specific metabolic traits.

Strains across the Lactobacillaceae family form the basis for a trillion-dollar industry. Our understanding of the genomic basis for their key traits is fragmented, however, including the metabolism that is foundational to their industrial uses. Pangenome analysis of publicly available Lactobacillaceae genomes allowed us to generate genome-scale metabolic network reconstructions for 26 species of industrial importance. Their manual curation led to more than 75,000 gene-protein-reaction associations that were deployed to generate 2,446 genome-scale metabolic models. Cross-referencing genomes and known metabolic traits allowed for manual metabolic network curation and validation of the metabolic models. As a result, we provide the first pangenomic basis for metabolism in the Lactobacillaceae family and a collection of predictive computational metabolic models that enable a variety of practical uses.IMPORTANCELactobacillaceae, a bacterial family foundational to a trillion-dollar industry, is increasingly relevant to biosustainability initiatives. Our study, leveraging approximately 2,400 genome sequences, provides a pangenomic analysis of Lactobacillaceae metabolism, creating over 2,400 curated and validated genome-scale models (GEMs). These GEMs successfully predict (i) unique, species-specific metabolic reactions; (ii) niche-enriched reactions that increase organism fitness; (iii) essential media components, offering insights into the global amino acid essentiality of Lactobacillaceae; and (iv) fermentation capabilities across the family, shedding light on the metabolic basis of Lactobacillaceae-based commercial products. This quantitative understanding of Lactobacillaceae metabolic properties and their genomic basis will have profound implications for the food industry and biosustainability, offering new insights and tools for strain selection and manipulation.

Genome-wide identification of ATG genes and their expression profiles under biotic and abiotic stresses in Fenneropenaeus chinensis

BackgroundAutophagy is a conserved catabolic process in eukaryotes that contributes to cell survival in response to multiple stresses and is important for organism fitness. Extensive research has shown that autophagy plays a pivotal role in both viral infection and replication processes. Despite the increasing research dedicated to autophagy, investigations into shrimp autophagy are relatively scarce.ResultsBased on three different methods, a total of 20 members of the ATGs were identified from F. chinensis, all of which contained an autophagy domain. These genes were divided into 18 subfamilies based on their different C-terminal domains, and were found to be located on 16 chromosomes. Quantitative real-time PCR (qRT-PCR) results showed that ATG genes were extensively distributed in all the tested tissues, with the highest expression levels were detected in muscle and eyestalk. To clarify the comprehensive roles of ATG genes upon biotic and abiotic stresses, we examined their expression patterns. The expression levels of multiple ATGs showed an initial increase followed by a decrease, with the highest expression levels observed at 6 h and/or 24 h after WSSV injection. The expression levels of three genes (ATG1, ATG3, and ATG4B) gradually increased until 60 h after injection. Under low-salt conditions, 12 ATG genes were significantly induced, and their transcription abundance peaked at 96 h after treatment.ConclusionsThese results suggested that ATG genes may have significant roles in responding to various environmental stressors. Overall, this study provides a thorough characterization and expression analysis of ATG genes in F. chinensis, laying a strong foundation for further functional studies and promising potential in innate immunity.

Biomarkers for aging in Caenorhabditis elegans high throughput screening.

Aging is characterized by a functional decline in organism fitness over time due to a complex combination of genetic and environmental factors [ 1-4]. With an increasing elderly population at risk of age-associated diseases, there is a pressing need for research dedicated to promoting health and longevity through anti-aging interventions. The roundworm Caenorhabditis elegans is an established model organism for aging studies due to its short life cycle, ease of culture, and conserved aging pathways. These benefits also make the worm well-suited for high-throughput screening (HTS) methods to study biomarkers of the molecular changes, cellular dysfunction, and physiological decline associated with aging. Within this review, we offer a summary of recent advances in HTS techniques to study biomarkers of aging in C. elegans.

Synthetic genomes unveil the effects of synonymous recoding.

Engineering the genetic code of an organism provides the basis for (i) making any organism safely resistant to natural viruses and (ii) preventing genetic information flow into and out of genetically modified organisms while (iii) allowing the biosynthesis of genetically encoded unnatural polymers1-4. Achieving these three goals requires the reassignment of multiple of the 64 codons nature uses to encode proteins. However, synonymous codon replacement-recoding-is frequently lethal, and how recoding impacts fitness remains poorly explored. Here, we explore these effects using whole-genome synthesis, multiplexed directed evolution, and genome-transcriptome-translatome-proteome co-profiling on multiple recoded genomes. Using this information, we assemble a synthetic Escherichia coli genome in seven sections using only 57 codons to encode proteins. By discovering the rules responsible for the lethality of synonymous recoding and developing a data-driven multi-omics-based genome construction workflow that troubleshoots synthetic genomes, we overcome the lethal effects of 62,007 synonymous codon swaps and 11,108 additional genomic edits. We show that synonymous recoding induces transcriptional noise including new antisense RNAs, leading to drastic transcriptome and proteome perturbation. As the elimination of select codons from an organism's genetic code results in the widespread appearance of cryptic promoters, we show that synonymous codon choice may naturally evolve to minimize transcriptional noise. Our work provides the first genome-scale description of how synonymous codon changes influence organismal fitness and paves the way for the construction of functional genomes that provide genetic firewalls from natural ecosystems and safely produce biopolymers, drugs, and enzymes with an expanded chemistry.

Amorosia littoralis Mantle & D. Hawksw. survives as root endophyte of mangroves and produces water soluble melanin pigment

Melanins are heterogenous biopolymers produced by many macro and microorganisms. They enhance the ecological fitness of the producer organisms by improving their virulence and protecting them from radiation, osmotic and heat stresses. Fungi synthesise either DOPA or DHN melanin and deposit them on their cell walls. Some fungal isolates produce water soluble melanin (pyomelanin) which is excerted out of the hyphae into the surrounding environment. Pyomelanin, a polymer of homogentisate, exhibits antimicrobial, UV screening, antioxidative, and anti-inflammatory activities and recent studies also show that pyomelanin could find use in space travel as radiation shield. However, scant literature is available on fungi with ability to produce pyomelanin. We report for the first time that Amorosia littoralis occurs as a root endophyte in mangrove species including Avicennia marina, Bruguiera cylindrica and Bruguiera gymnorhiza and produces pyomelanin. Considering the various technological uses of pyomelanin, this study underscores the need to explore fungi of different habitats to identify hyperproducers and to obtain chemically diverse pyomelanin.

Differential Toxicity of Arsenic in Daphnia pulex Under Phosphorus and Food Limitation.

The on-going anthropogenic degradation of freshwater habitats has drastically altered the environmental supply of both nutrients and common pollutants. Most organisms living in these altered habitats experience interactive effects of various stressors that can initiate adjustments at multiple levels impacting their fitness. Hence, studies measuring response to a single environmental parameter fail to capture the complexities of the status quo. We tested both the individual and the interactive effect of arsenic (As) exposure, food quantity, and dietary phosphorus (P)-supply on six life-history traits (Juvenile Growth Rate; Adult Growth Rate; Age and Size at Maturity, Lifespan, and Fecundity) as surrogates for organismal fitness in the keystone aquatic grazer Daphnia pulex. We also tested the effect of food quantity and P-supply on somatic As accumulation in Daphnia. Our results indicated an influence of P-supply on neonatal growth and an influence of As and food quantity on growth and maintenance later in life. Maturation was strongly influenced by all three variables, with no reproduction observed in the presence of two or more environmental stressors. We found a strong interaction between As and dietary P, with increased P-supply intensifing the toxicity effect of As. No such effects were seen between As and food quantity, indicating a differential role of quantity versus quality on As toxicity. We found a nominal effect of diet on somatic As accumulation. The results from the present study emphasize the importance of considering such interactions between co-occurring environmental stressors and the dietary status of organisms, to better predict and manage impacts and risks associated with common environmental toxicants in highly vulnerable ecosystems. Environ Toxicol Chem 2024;43:1807-1819. © 2024 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Demographic effects of aggregation in the presence of a component Allee effect.

The component Allee effect (AE) is the positive correlation between an organism's fitness component and population density. Depending on the population spatial structure, which determines the interactions between organisms, a component AE might lead to positive density dependence in the population per-capita growth rate and establish a demographic AE. However, existing spatial models impose a fixed population spatial structure, which limits the understanding of how a component AE and spatial dynamics jointly determine the existence of demographic AEs. We introduce a spatially explicit theoretical framework where spatial structure and population dynamics are emergent properties of the individual-level demographic and movement rates. This framework predicts various spatial patterns depending on its specific parametrization, including evenly spaced aggregates of organisms, which determine the demographic-level by-products of the component AE. We find that aggregation increases population abundance and allows population survival in harsher environments and at lower global population densities when compared with uniformly distributed organisms. Moreover, aggregation can prevent the component AE from manifesting at the population level or restrict it to the level of each independent aggregate. These results provide a mechanistic understanding of how component AEs might operate for different spatial structures and manifest at larger scales.

Weak neuronal glycolysis sustains cognition and organismal fitness

The energy cost of neuronal activity is mainly sustained by glucose1,2. However, in an apparent paradox, neurons modestly metabolize glucose through glycolysis3–6, a circumstance that can be accounted for by the constant degradation of 6-phosphofructo-2-kinase–fructose-2,6-bisphosphatase-3 (PFKFB3)3,7,8, a key glycolysis-promoting enzyme. To evaluate the in vivo physiological importance of this hypoglycolytic metabolism, here we genetically engineered mice with their neurons transformed into active glycolytic cells through Pfkfb3 expression. In vivo molecular, biochemical and metabolic flux analyses of these neurons revealed an accumulation of anomalous mitochondria, complex I disassembly, bioenergetic deficiency and mitochondrial redox stress. Notably, glycolysis-mediated nicotinamide adenine dinucleotide (NAD+) reduction impaired sirtuin-dependent autophagy. Furthermore, these mice displayed cognitive decline and a metabolic syndrome that was mimicked by confining Pfkfb3 expression to hypothalamic neurons. Neuron-specific genetic ablation of mitochondrial redox stress or brain NAD+ restoration corrected these behavioural alterations. Thus, the weak glycolytic nature of neurons is required to sustain higher-order organismal functions.