Levels Of Biological Organization Research Articles

Modularity and connectivity of nest structure scale with colony size.

Large body sizes have evolved structures to facilitate resource transport. Like unitary organisms, social insect colonies must transport information and resources. Colonies with more individuals may experience transport challenges similar to large-bodied organisms. In ant colonies, transport occurs in the nest, which may consist of structures that facilitate movement. We examine three attributes of nests that might have evolved to mitigate transport challenges related to colony size: (1) subdivision-nests of species with large colonies are more subdivided to reduce crowd viscosity; (2) branching-nest tunnels increase branching in species with large colonies to reduce travel distances; and (3) shortcuts-nests of species with large colonies have cross-linking tunnels to connect distant parts of the nest and create alternative routes. We test these hypotheses by comparing nest structures of species with different colony sizes in phylogenetically controlled meta-analyses. Our findings support the hypothesis that nest subdivision and branching evolved to mitigate transport challenges related to colony size. Nests of species with large colonies contain more chambers and branching tunnels. The similarity in how ant nests and bodies of unitary organisms have evolved in response to increasing size suggests common solutions across taxa and levels of biological organization.

Integrative Analysis of Molecular and Physiological Data to Quantify Biological Aging

Development of reliable and valid measurements to quantify biological aging is a critical frontier geroscience. Originating in accumulations of molecular changes, biological aging undermines resilience within cellular networks and organ systems, driving disease, disability, and mortality. Measurements of biological aging have been proposed at several molecular and physiological levels of analysis. But agreement between measures implemented at different levels of analysis is low. The timing at which aging processes manifest at different levels of biological organization may vary, with the result that signs of aging manifest in one level of analysis are not yet observable in another. And different aging processes may be most apparent in different molecular levels of analysis. In midlife humans, aging-related changes are manifest at multiple molecular and physiological levels, making this population ideal for development of measurements that integrate information across levels of analysis to more precisely quantify the state and pace of biological aging.

Fungi as mediators linking organisms and ecosystems.

ABSTRACTFungi form a major and diverse component of most ecosystems on Earth. They are both micro and macroorganisms with high and varying functional diversity as well as great variation in dispersal modes. With our growing knowledge of microbial biogeography, it has become increasingly clear that fungal assembly patterns and processes differ from other microorganisms such as bacteria, but also from macroorganisms such as plants. The success of fungi as organisms and their influence on the environment lies in their ability to span multiple dimensions of time, space, and biological interactions, that is not rivalled by other organism groups. There is also growing evidence that fungi mediate links between different organisms and ecosystems, with the potential to affect the macroecology and evolution of those organisms. This suggests that fungal interactions are an ecological driving force, interconnecting different levels of biological and ecological organisation of their hosts, competitors, and antagonists with the environment and ecosystem functioning. Here we review these emerging lines of evidence by focusing on the dynamics of fungal interactions with other organism groups across various ecosystems. We conclude that the mediating role of fungi through their complex and dynamic ecological interactions underlie their importance and ubiquity across Earth's ecosystems.

Multiscale Brain Aging in the Context of Neurodegeneration and Alzheimer's Disease

The brain, with a diverse array of specialized cells, regional substructures, and a relatively isolated microenvironment, represents a uniquely challenging organ system for aging research. The brain can experience physical trauma, interact with the periphery, and is responsible for cognitive and behavioral modifications that can feed back into the molecular processes of aging both within and external to the brain. Advances to our understanding and ability to intervene in the complexity that personifies brain aging and associated neurodegeneration will require integrated, multiscale approaches operating in tandem. Therefore, we have organized this symposium to highlight promising new approaches to study brain aging through the lens of multiple biological levels of organization. We will provide insight not only into normal brain aging, but will also suggest key spurious processes that may drive neurodegeneration and functional decline.

Biomarker Studies in Stress Biology: From the Gene to Population, from the Organism to the Application.

Simple SummaryEcosystems have been increasingly subject to stressful conditions and thus the need to develop tools capable of assessing their impacts on populations and communities. These effects assessed at higher levels of biological organization tend to reflect the sum of effects on individuals, arising from the effects at the cellular and molecular levels. These lower biological organization levels are more responsive at an early stage, allowing them to be used as early warning endpoints to address environmental stress—biomarkers. In this work, the need to link low to high levels of biological organization is addressed and the challenges and usefulness of biomarkers in a myriad of fields discussed.Endpoints assessed at the population or community level are most often the result of the sum of effects on individuals, arising from the effects at the cellular and molecular levels. Within this framework, these lower biological level endpoints are more responsive at an early stage of exposure, making them potential toolboxes to be used as early-warning markers to address stress. Given this, by linking responses and understanding organisms’ metabolism and physiology, the possibilities for the use of biomarkers in stress biology are vast. Here, biomarker comprehensive examples are given to enlighten the need to link levels of biological organization, and their usefulness for a myriad of fields and applications is presented and discussed.

Assessment of the juvenile vulnerability of symbiont-bearing giant clams to ocean acidification

Ocean acidification (OA) severely affects marine bivalves, especially their calcification processes. However, very little is known about the fate of symbiont-bearing giant clams in the acidified oceans, which hinders our ability to develop strategies to protect this ecologically and economically important group in coral reef ecosystems. Here, we explored the integrated juvenile responses of fluted giant clam Tridacna squamosa (Lamarck, 1819) to acidified seawater at different levels of biological organization. Our results revealed that OA did not cause a significant reduction in survival and shell growth performance, indicating that T. squamosa juveniles are tolerated to moderate acidification. Yet, significantly reduced net calcification rate demonstrated the calcifying physiology sensitivity to OA, in line with significant declines in symbiont photosynthetic yield and zooxanthellae density which in turn lowered the amount of energy supply for energetically expensive calcification processes. Subsequent transcriptome sequencing and comparative analysis of differentially expressed genes revealed that the regulation of calcification processes, such as transport of calcification substrates, acid-base regulation, synthesis of organic matrix in the calcifying fluid, as well as metabolic depression were the major response to OA. Taken together, the integration of physiological and molecular responses can provide a comprehensive understanding of how the early life history stages of giant clams respond to OA and make an important leap forward in assessing their fate under future ocean conditions.

Marine research and management topics addressed by process-based ecosystem models

The earth’s oceans and ecosystems face climatic changes and multiple anthropogenic stressors. In the face of this, managers of the marine environment are increasingly adopting the ecosystem approach to underpin their decision making. Process-based ecosystem models (frequently referred to as dynamic models) synthesize existing observational and experimental knowledge into a numerical framework, but an obstacle to the incorporation of these models in management is the lack of credibility due to limited control of uncertainty in the results. The 13 papers in this Theme Section highlight how ecosystem models are, or can be, applied as management tools, and the various ways in which they quantify uncertainty and evaluate the skill. The papers span all levels of biological organization from individuals to populations and ecosystems, and cover a wide selection of anthropogenic pressures. Bearing in mind that the interpretation of observations is in fact also a model with representativeness error, we advocate a closer combination of observations and models to bring both methods forward. With the current challenges to the marine ecosystem and our uses of it, the more tools marine managers have in their ‘toolbox’, the better; dynamic modelling is one such very important tool, and its inclusion in ecosystem management should be continuously assessed.

Temperature-dependence of metabolism and fuel selection from cells to whole organisms.

Temperature affects nearly every aspect of how organisms interact with and are constrained by their environment. Measures of organismal energetics, such as metabolic rate, are highly temperature-dependent and governed through temperature effects on rates of biochemical reactions. Characterizing the relationships among levels of biological organization can lend insight into how temperature affects whole-organism function. We tested the temperature dependence of cellular oxygen consumption and its relationship to whole-animal metabolic rate in garter snakes (Thamnophis elegans). Additionally, we tested whether thermal responses were linked to shifts in the fuel source oxidized to support metabolism with the use of carbon stable isotopes. Our results demonstrate temperature dependence of metabolic rates across levels of biological organization. Cellular (basal, adenosine triphosphate-linked) and whole-animal rates of respiration increased with temperature but were not correlated within or among individuals, suggesting that variation in whole-animal metabolic rates is not due simply to variation at the cellular level, but rather other interacting factors across scales of biological organization. Counter to trends observed during fasting, elevated temperature did not alter fuel selection (i.e., natural-abundance stable carbon isotope composition in breath, δ13 Cbreath ). This consistency suggests the maintenance and oxidation of a single fuel source supporting metabolism across a broad range of metabolic demands.

Physiological Performance Curves: When Are They Useful?

This review serves as an introduction to a special issue of Frontiers in Physiology, focused on the importance of physiological performance curves across phylogenetic and functional boundaries. Biologists have used performance curves to describe the effects of changing environmental conditions on animal physiology since the late 1800s (at least). Animal physiologists have studied performance curves extensively over the past decades, and there is a good foundation to understanding how the environment affects physiological functions of individuals. Our goal here was to build upon this research and address outstanding questions regarding the mutability and applicability of performance curves across taxonomic groups and levels of biological organization. Performance curves are not fixed at a taxonomic, population, or individual level – rather they are dynamic and can shift in response to evolutionary pressures (e.g., selection) and epigenetic programming (e.g., plasticity). The mechanisms underlying these shifts are being increasingly used to predict the efficacy with which plasticity and heritability of performance curves can render individuals and populations less vulnerable to climate change. Individual differences in physiological performance curves (and plasticity of performance curves) can also have cascading effects at higher levels of biological organization. For instance, individual physiology likely influences group behaviors in non-additive ways. There is a need therefore to extend the concept of performance curves to social interactions and sociality. Collectively, this special issue emphasizes the power of how within- and between-individual shifts in performance curves might scale up to the population-, species-, and community-level dynamics that inform conservation management strategies.

A multifaceted assessment of the effects of polyethylene microplastics on juvenile gilthead seabreams (Sparus aurata).

Plastic pollution has become a major environmental and societal concern in the last decade. From larger debris to microplastics (MP), this pollution is ubiquitous and particularly affects aquatic ecosystems. MP can be directly or inadvertently ingested by organisms, transferred along the trophic chain, and sometimes translocated into tissues. However, the impacts of such MP exposure on organisms' biological functions are yet to be fully understood. Here, we used a multi-diagnostic approach at multiple levels of biological organization (from atoms to organisms) to determine how MP affect the biology of a marine fish, the gilthead seabream, Sparus aurata. We exposed juvenile seabreams for 35 days to spherical 10-20µm polyethylene primary MP through food (Artemia salina pre-exposed to MP) at a concentration of 5±1µg of MP per gram of fish per day. MP-exposed fish experienced higher mortality, increased abundance of several brain and liver primary metabolites, hepatic and intestinal histological defects, higher assimilation of an essential element (Zn), and lower assimilation of a non-essential element (Ag). In contrast, growth and muscle C/N isotopic profiles were similar between control and MP-exposed fish, while variable patterns were observed for the intestinal microbiome. This comprehensive analysis of biological responses to MP exposure reveals how MP ingestion can cause negligible to profound effects in a fish species and contributes towards a better understanding of the causal mechanisms of its toxicity.

Environmental optima for an ecosystem engineer: a multidisciplinary trait-based approach

A complex interplay of biotic and abiotic factors underpins the distribution of species and operates across different levels of biological organization and life history stages. Understanding ecosystem engineer reproductive traits is critical for comprehending and managing the biodiversity-rich habitats they create. Little is known about how the reproduction of the reef-forming worm, Sabellaria alveolata, varies across environmental gradients. By integrating broad-scale environmental data with in-situ physiological data in the form of biochemical traits, we identified and ranked the drivers of intraspecific reproductive trait variability (ITV). ITV was highest in locations with variable environmental conditions, subjected to fluctuating temperature and hydrodynamic conditions. Our trait selection pointed to poleward sites being the most physiologically stressful, with low numbers of irregularly shaped eggs suggesting potentially reduced reproductive success. Centre-range individuals allocated the most energy to reproduction, with the highest number of intermediate-sized eggs, whilst equatorward sites were the least physiologically stressful, thus confirming the warm-adapted nature of our model organism. Variation in total egg diameter and relative fecundity were influenced by a combination of environmental conditions, which changed depending on the trait and sampling period. An integrated approach involving biochemical and reproductive traits is essential for understanding macro-scale patterns in the face of anthropogenic-induced climate change across environmental and latitudinal gradients.

The evolution of germ-soma specialization under different genetic and environmental effects

Division of labor exists at different levels of biological organization – from cell colonies to human societies. One of the simplest examples of the division of labor in multicellular organisms is germ-soma specialization, which plays a key role in the evolution of organismal complexity. Here we formulate and study a general mathematical model exploring the emergence of germ-soma specialization in colonies of cells. We consider a finite population of colonies competing for resources. Colonies are of the same size and are composed by asexually reproducing haploid cells. Each cell can contribute to activity and fecundity of the colony, these contributions are traded-off. We assume that all cells within a colony are genetically identical but gene effects on fecundity and activity are influenced by variation in the microenvironment experienced by individual cells. Through analytical theory and evolutionary agent-based modeling we show that the shape of the trade-off relation between somatic and reproductive functions, the type and extent of variation in within-colony microenvironment, and, in some cases, the number of genes involved, are important predictors of the extent of germ-soma specialization. Specifically, increasing convexity of the trade-off relation, the number of different environmental gradients acting within a colony, and the number of genes (in the case of random microenvironmental effects) promote the emergence of germ-soma specialization. Overall our results contribute towards a better understanding of the role of genetic, environmental, and microenvironmental factors in the evolution of germ-soma specialization.

Fat on plastic: Metabolic consequences of an LDPE diet in the fat body of the greater wax moth larvae (Galleria mellonella)

The caterpillar larvae of the greater wax moth (Galleria mellonella) are avid plastivores, as when provided a diet of low-density polyethylene (LDPE) they actively feed on it. Recent work has highlighted the importance of their microbiome in the putative biodegradation of this plastic polymer, though the impact of plastic metabolism on the insect host is less clear. In the present study, we undertook an integrative approach spanning all levels of biological organization to explore the effects of a plastic diet on the metabolic physiology of this animal model of plastic biodegradation. We demonstrate that an LDPE diet is not sufficient to maintain optimal larval growth and survival. In addition, we confirm that plastic fed waxworms retain their fat body lipid stores in a manner proportional to their individual polyethylene consumption suggesting a direct effect of LDPE biodegradation. At the functional level, the oxidative capacity of the fat body of LDPE-fed larvae is maintained reflecting unaltered metabolic function of the tissue. Finally, metabolomic analyses confirmed fat body lipid stores maintenance in LDPE-fed worms, but uncovered various other nutritional deficiencies. Overall, this work unveils novel insights in the complex interplay between LDPE biodegradation and the metabolic physiology of this model plastivore.

Plumbojarosite Remediation of Soil Affects Lead Speciation and Elemental Interactions in Soil and in Mice Tissues.

Lead (Pb) contamination of soils is of global concern due to the devastating impacts of Pb exposure in children. Because early-life exposure to Pb has long-lasting health effects, reducing exposure in children is a critical public health goal that has intensified research on the conversion of soil Pb to low bioavailability phases. Recently, plumbojarosite (PLJ) conversion of highly available soil Pb was found to decrease Pb relative bioavailability (RBA <10%). However, there is sparse information concerning interactions between Pb and other elements when contaminated soil, pre- and post-remediation, is ingested and moves through the gastrointestinal tract (GIT). Addressing this may inform drivers of effective chemical remediation strategies. Here, we utilize bulk and micro-focused Pb X-ray absorption spectroscopy to probe elemental interactions and Pb speciation in mouse diet, cecum, and feces samples following ingestion of contaminated soils pre- and post-PLJ treatment. RBA of treated soils was less than 1% with PLJ phases transiting the GIT with little absorption. In contrast, Pb associated with organics was predominantly found in the cecum. These results are consistent with transit of insoluble PLJ to feces following ingestion. The expanded understanding of Pb interactions during GIT transit complements our knowledge of elemental interactions with Pb that occur at higher levels of biological organization.

Temperature effects on community size structure: The value of large-scale biomonitoring programs.

The effects of climate warming on individuals and populations are becoming increasingly apparent (e.g. changes in body mass, species range shifts), however impacts at higher levels of biological organization (i.e. communities and ecosystems) are less understood (Heneghan et al., 2019). Ecological communities comprise many small and few large sized individuals.

Investigating the impact of remediation efforts on Hedistediversicolor in the Seine estuary using multiple levels of biological organization

The Seine Estuary is historically one of the most contaminated estuaries in Europe. In 2002 the estuary underwent major redevelopment which emphasized environmental remediation to measure biological effects. The present study investigated the health status of the sentinel species Hediste diversicolor in the Seine estuary by comparing data from a sampling campaign immediately after the Seine underwent reconstruction and 10 years afterward. Both studies implemented multiple levels of biological organization ranging from enzymatic biomarkers to population density. Integrative modeling was used to establish a holistic status assessment for H. diversicolor in the Seine. H. diversicolor populations in the Seine estuary were impacted in both campaigns suggesting no significant improvements over the 10-year period. This interpretation however can be improved by increasing the number of reference sites used to establish the baseline natural variation, integrating additional environmental parameters into the model and measuring additional biological endpoints, such as reproductive status.

Combined effects of heatwaves and micropollutants on freshwater ecosystems: Towards an integrated assessment of extreme events in multiple stressors research.

Freshwater ecosystems are strongly influenced by weather extremes such as heatwaves (HWs), which are predicted to increase in frequency and magnitude in the future. In addition to these climate extremes, the freshwater realm is impacted by the exposure to various classes of chemicals emitted by anthropogenic activities. Currently, there is limited knowledge on how the combined exposure to HWs and chemicals affects the structure and functioning of freshwater ecosystems. Here, we review the available literature describing the single and combined effects of HWs and chemicals on different levels of biological organization, to obtain a holistic view of their potential interactive effects. We only found a few studies (13 out of the 61 studies included in this review) that investigated the biological effects of HWs in combination with chemical pollution. The reported interactive effects of HWs and chemicals varied largely not only within the different trophic levels but also depending on the studied endpoints for populations or individuals. Hence, owing also to the little number of studies available, no consistent interactive effects could be highlighted at any level of biological organization. Moreover, we found an imbalance towards single species and population experiments, with only five studies using a multitrophic approach. This results in a knowledge gap for relevant community and ecosystem level endpoints, which prevents the exploration of important indirect effects that can compromise food web stability. Moreover, this knowledge gap impairs the validity of chemical risk assessments and our ability to protect ecosystems. Finally, we highlight the urgency of integrating extreme events into multiple stressors studies and provide specific recommendations to guide further experimental research in this regard.

Reshaping the Tree of Life: ecological implications of evolution in the Anthropocene

Novel in their scope and intensity, human‐mediated changes in genetic diversity through directed gene transfer technologies and longer standing human‐driven selective pressures, such as land‐use change, species introductions, mass extinctions, and broad application of antibiotics, are combining to reorganize mechanisms of evolution. The evolutionary consequences of anthropogenic change can be observed across levels of biological organization and are influencing the rate of micro‐ and macroevolutionary changes, as well as feedback among them. This may have large‐scale effects on the provisioning of ecosystem services, food security, and human health. Here, we summarize several of the ecological implications of human modification of evolutionary dynamics, focusing specifically on emerging molecular technologies, to highlight some of the challenges in predicting subsequent changes in the world’s ecosystems.

Network analysis reveals rare disease signatures across multiple levels of biological organization

Rare genetic diseases are typically caused by a single gene defect. Despite this clear causal relationship between genotype and phenotype, identifying the pathobiological mechanisms at various levels of biological organization remains a practical and conceptual challenge. Here, we introduce a network approach for evaluating the impact of rare gene defects across biological scales. We construct a multiplex network consisting of over 20 million gene relationships that are organized into 46 network layers spanning six major biological scales between genotype and phenotype. A comprehensive analysis of 3,771 rare diseases reveals distinct phenotypic modules within individual layers. These modules can be exploited to mechanistically dissect the impact of gene defects and accurately predict rare disease gene candidates. Our results show that the disease module formalism can be applied to rare diseases and generalized beyond physical interaction networks. These findings open up new venues to apply network-based tools for cross-scale data integration.

Trade-Offs (and Constraints) in Organismal Biology

AbstractTrade-offs and constraints are inherent to life, and studies of these phenomena play a central role in both organismal and evolutionary biology. Trade-offs can be defined, categorized, and studied in at least six, not mutually exclusive, ways. (1) Allocation constraints are caused by a limited resource (e.g., energy, time, space, essential nutrients), such that increasing allocation to one component necessarily requires a decrease in another (if only two components are involved, this is referred to as the Y-model, e.g., energy devoted to size versus number of offspring). (2) Functional conflicts occur when features that enhance performance of one task decrease performance of another (e.g., relative lengths of in-levers and out-levers, force-velocity trade-offs related to muscle fiber type composition). (3) Shared biochemical pathways, often involving integrator molecules (e.g., hormones, neurotransmitters, transcription factors), can simultaneously affect multiple traits, with some effects being beneficial for one or more components of Darwinian fitness (e.g., survival, age at first reproduction, fecundity) and others detrimental. (4) Antagonistic pleiotropy describes genetic variants that increase one component of fitness (or a lower-level trait) while simultaneously decreasing another. (5) Ecological circumstances (or selective regime) may impose trade-offs, such as when foraging behavior increases energy availability yet also decreases survival. (6) Sexual selection may lead to the elaboration of (usually male) secondary sexual characters that improve mating success but handicap survival and/or impose energetic costs that reduce other fitness components. Empirical studies of trade-offs often search for negative correlations between two traits that are the expected outcomes of the trade-offs, but this will generally be inadequate if more than two traits are involved and especially for complex physiological networks of interacting traits. Moreover, trade-offs often occur only in populations that are experiencing harsh environmental conditions or energetic challenges at the extremes of phenotypic distributions, such as among individuals or species that have exceptional athletic abilities. Trade-offs may be (partially) circumvented through various compensatory mechanisms, depending on the timescale involved, ranging from acute to evolutionary. Going forward, a pluralistic view of trade-offs and constraints, combined with integrative analyses that cross levels of biological organization and traditional boundaries among disciplines, will enhance the study of evolutionary organismal biology.