Consequences Of Individual Variation Research Articles

Simulating individual movement in fish

Accurately quantifying an animal’s movement is crucial for developing a greater empirical and theoretical understanding of its behaviour, and for simulating biologically plausible movement patterns. However, we have a relatively poor understanding of how animals move at fine temporal scales and in three-dimensional environments. Here, we collected high temporal resolution data on the three-dimensional spatial positions of individual three-spined sticklebacks (Gasterosteus aculeatus), allowing us to derive statistics describing key geometric characteristics of their movement and to quantify the extent to which this varies between individuals. We then used these statistics to develop a simple model of fish movement and evaluated the biological plausibility of simulated movement paths using a Turing-type test, which quantified the association preferences of live fish towards animated conspecifics following either ‘real’ (i.e., based on empirical measurements) or simulated movements. Live fish showed no difference in their response to ‘real’ movement compared to movement simulated by the model, although significantly preferred modelled movement over putatively unnatural movement patterns. The model therefore has the potential to facilitate a greater understanding of the causes and consequences of individual variation in movement, as well as enabling the construction of agent-based models or real-time computer animations in which individual fish move in biologically feasible ways.

Chiral pharmacokinetics of ibuprofen enantiomers in Chinese preterm neonates with patent ductus arteriosus using a validated UHPLC-MS/MS method

Persistent patent ductus arteriosus (PDA) is generally observed in preterm neonates. Oral ibuprofen is the standard treatment for closing PDA in China. To investigate the chiral pharmacokinetics of ibuprofen enantiomers in Chinese premature infants with PDA, a simple, fast, and sensitive analytical enantioselective technology was developed with ultra-performance liquid chromatography (UPLC) – tandem mass spectrometry (MS/MS). Chromatographic separation of (R)-ibuprofen and (S)-ibuprofen was accomplished on a Lux® 3 µm Cellulose-3 (150 mm × 2.0 mm, 3 μm) at a flow rate of 0.2 mL/min within 6 min. UPLC separation was achieved by isocratic elution with a mobile phase consisting of formic acid:water (75:1000000, v/v) and acetonitrile:methanol (1:1, v/v). Only 50 µL of plasma samples were pre-treated with acetonitrile precipitation. Ibuprofen-d3 was used as an internal standard. The standard curves of both enantiomers were linear over a concentration range of 0.0500 μg/mL to 50.00 μg/mL. The method has been validated for selectivity, carryover effect, lower limit of quantification, precision, accuracy, matrix effect, extraction recovery, dilution integrity, and stability based on the existing guidelines of the National Medical Products Administration, the United States Food and Drug Administration, and the European Medicines Agency. This method has been successfully applied to investigate the pharmacokinetics of ibuprofen enantiomers in 9 preterm infants with PDA. Our results showed that a high chiral inversion ratio of (R)- to (S)-ibuprofen exists in Chinese preterm neonates. Further studies should be conducted to monitor drug concentration following oral administration of ibuprofen and to consider the effect of individual variations and ethnic differences in metabolizing enantiomers of ibuprofen in premature neonates with PDA.

Workload Distribution and Division of Labor in Cooperative Societies

Cooperative groups are ubiquitous in animals, as are the challenges of allocating labor to accomplish cooperative tasks, including territory defense, hunting, and brood care. Individual contributions can differ in two ways, both of which can influence fitness: group members can vary in overall helpfulness (workload) or they can specialize on different tasks (division of labor). In this review, we encourage additional, simultaneous study of both workload distribution and division of labor. Historically, workload distribution has been studied in the contexts of collective action and cooperative offspring care. Both areas of research aim to understand how shared benefits can emerge from individual contributions, but they remain poorly integrated. We argue that each of these literatures has strengths that could benefit the other, and we highlight potential areas of crosstalk. Next, we review the literature on division of labor in taxa other than the eusocial insects, discuss parallels and differences in division of labor between eusocial insects and other animals, and encourage more work on cooperative, noninsect taxa. Rigorous work on individual contributions to cooperative tasks will expand our understanding of the causes and consequences of individual variation and the evolutionary stability of social living.

Plant height and spatial context influence individual connectivity and specialization on seed dispersers in a tree population.

While network analyses have stimulated a renewed interest in understanding patterns and drivers of specialization within communities, few studies have explored specialization within populations. Thus, in plant populations, causes and consequences of individual variation in their interactions with mutualistic animals remain poorly understood. Studying a Brazilian pepper (Schinus terebinthifolia) population, we measured the extent of individual variation in interactions with seed dispersers and tested whether connectivity (number of seed dispersers) and specialization (exclusiveness of partners) are associated with phenotypic and phenological traits of individuals and their spatial context. We found that: (i) individuals varied broadly in their connectivity and specialization on seed dispersers; (ii) phenotypic traits and spatial context matter more than fruiting duration in determining how many and how exclusive are seed dispersers of an individual; (iii) the individual-based network was nested and indicated that the less connected individuals were shorter, occurred in neighborhoods with fewer fruits, and tended to interact with a subset of the partners of more generalist individuals which, in turn, were taller and inserted in higher fruit density neighborhoods; (iv) modularity indicated the existence of subsets of individuals that interacted disproportionately with distinct groups of partners, which may occur due to differences in bird habitat use across the landscape. Our study underlines a remarkable interindividual variation that is overlooked when interactions are compiled to describe species-level interactions. Traits and spatial contexts that define variation among individuals may have important implications not only for fitness but also for sampling and description of interactions at species level.

Understanding why superspreading drives the COVID-19 pandemic but not the H1N1 pandemic

Understanding why superspreading drives the COVID-19 pandemic but not the H1N1 pandemic

Variation among stallions in sperm quality after single layer centrifugation

Although single layer centrifugation (SLC) selects robust spermatozoa from stallion semen, the effect of individual variation has not been studied in detail. The objective of this study was to determine the variation among stallions in the effects of SLC on sperm quality during cooled storage for up to 48hr. Semen samples from seven stallions (18 ejaculates) were split, with one portion being used for SLC and the other serving as a control (CON). Sperm quality (kinematics, reactive oxygen species (ROS) production, membrane integrity (MI) and chromatin integrity) were analysed at 0, 24 and 48hr using computer-assisted sperm analysis and flow cytometry. Sperm quality was better in SLC than in CON at all timepoints, especially chromatin integrity and MI (p<.0001 for both), and some categories of ROS production (e.g. proportion of live hydrogen peroxide negative spermatozoa, p<.0001), but the degree of improvement varied among stallions and type of ROS (p<.05-p<.0001). Total and progressive motility were also better in SLC samples than in CON at 24 and 48hr (p<.0001), although the effect on sperm kinematics varied. The interaction of treatment, time and stallion was not significant. In conclusion, sperm quality was better in SLC samples than in CON, although there was considerable individual variation among stallions. The improvement in sperm quality, particularly in chromatin integrity, was clearly beneficial, and therefore the use of this technique would be warranted for all stallion semen samples.

Variation of social strategies within and between individual black-tailed prairie dogs (Cynomys ludovicianus) during the reproductive season

Sociality describes the tendency for members of a species to associate in a group based on social attraction. To balance the trade-offs of sociality, the fitness consequences (and therefore proclivity towards being social) should be expected to vary across individuals and within the same individual, across time. We used social network analysis to evaluate the causes and consequences of within- and between-individual variation in sociality in a wild population of black-tailed prairie dogs (Cynomys ludovicianus) during the reproductive season. We hypothesised that individuals would adjust their behaviours based on a key life-history event: reproduction. We assessed this variation by comparing differences in social behaviour between individuals in different life history stages and within individuals across the reproductive season. We predicted breeding females would increase their agonistic interactions to protect their offspring from infanticide during reproduction, while non-reproductive individuals would increase their affiliative interactions to maintain stability in their social network and increase their indirect fitness. We found that the number of social interactions decreased after reproduction for all individuals. Breeding females did not increase their agonistic interactions compared to other groups, but instead had overall decreased social interactions during reproduction, which corresponded with increased fitness. For non-breeding females, an increase of affiliative social interactions correlated with increased indirect fitness as we predicted. Our multiple-level, temporally structured analyses revealed under-realised complexities regarding within- and between-individual variation in social interactions, suggesting reproductive status dictates different social strategies to optimise fitness. Social living with conspecifics confers a range of costs and benefits, the trade-offs of which are expected to change based on life history. Therefore, individuals should modulate their sociality across life history transitions to optimise fitness. Reproductive status is known to affect socio-behavioural decisions across taxa. We used a highly social species, black-tailed prairie dogs, to investigate variation in social structure across the reproductive season, and understand both the causes and consequences of individual variation in social structure. Prairie dogs offered easily observable, dynamic social behaviours and quantifiable fitness consequences to truly demonstrate acute social change. Our results suggest that there is variation of social interactions not only within individuals over time, but also between reproductive groups in the same time period. Our analyses suggest that social variation has important consequences for fitness and should further stimulate study of temporally based analyses of social behaviour.

Reptiles on the wrong track? Moving beyond traditional estimators with dynamic Brownian Bridge Movement Models

BackgroundAnimal movement expressed through home ranges or space-use can offer insights into spatial and habitat requirements. However, different classes of estimation methods are currently instinctively applied to answer home range, space-use or movement-based research questions regardless of their widely varying outputs, directly impacting conclusions. Recent technological advances in animal tracking (GPS and satellite tags), have enabled new methods to quantify animal space-use and movement pathways, but so far have primarily targeted mammal and avian species.MethodsMost reptile spatial ecology studies only make use of two older home range estimation methods: Minimum Convex Polygons (MCP) and Kernel Density Estimators (KDE), particularly with the Least Squares Cross Validation (LSCV) and reference (href) bandwidth selection algorithms. These methods are frequently applied to answer space-use and movement-based questions. Reptile movement patterns are unique (e.g., low movement frequency, long stop-over periods), prompting investigation into whether newer movement-based methods –such as dynamic Brownian Bridge Movement Models (dBBMMs)– apply to Very High Frequency (VHF) radio-telemetry tracking data. We simulated movement data for three archetypical reptile species: a highly mobile active hunter, an ambush predator with long-distance moves and long-term sheltering periods, and an ambush predator with short-distance moves and short-term sheltering periods. We compared traditionally used estimators, MCP and KDE, with dBBMMs, across eight feasible VHF field sampling regimes for reptiles, varying from one data point every four daylight hours, to once per month.ResultsAlthough originally designed for GPS tracking studies, dBBMMs outperformed MCPs and KDE href across all tracking regimes in accurately revealing movement pathways, with only KDE LSCV performing comparably at some higher frequency sampling regimes. However, the LSCV algorithm failed to converge with these high-frequency regimes due to high site fidelity, and was unstable across sampling regimes, making its use problematic for species exhibiting long-term sheltering behaviours. We found that dBBMMs minimized the effect of individual variation, maintained low error rates balanced between omission (false negative) and commission (false positive), and performed comparatively well even under low frequency sampling regimes (e.g., once a month).ConclusionsWe recommend dBBMMs as a valuable alternative to MCP and KDE methods for reptile VHF telemetry data, for research questions associated with space-use and movement behaviours within the study period: they work under contemporary tracking protocols and provide more stable estimates. We demonstrate for the first time that dBBMMs can be applied confidently to low-resolution tracking data, while improving comparisons across regimes, individuals, and species.

The standard metabolic rate of a land snail (Cepaea hortensis) is a repeatable trait and influences winter survival

Phenotypic selection on physiological parameters is an underrepresented topic in studies of evolutionary biology. There is especially a lack of studies involving invertebrate organisms. We studied the repeatability of the standard metabolic rate (SMR) and the effect of individual variation in SMR on the subsequent winter survival in a terrestrial shell-bearing mollusc, the white-lipped snail (Cepaea hortensis) in mid-Norway. SMR was measured twice during the autumn and – after an experimental overwintering at controlled conditions – twice during the following spring. We found a significant repeatability of SMR over all three time periods tested, with a clear effect of time, with a high repeatability of 0.56 over 4 days during spring, 0.44 over 12 days in the autumn and 0.17 over 194 days from autumn to spring. That SMR is a repeatable physiological trait across the winter period during which a possible selection might occur, suggests that SMR could be a potential target of natural selection. We indeed found that the autumn SMR significantly influenced the probability of survival during the winter period, with a combination of a positive linear (P = .011) and a quadratic stabilizing (P = .001) effect on SMR. Our results hence support the view that metabolic rate is an important physiological component influencing the fitness of an organism.

Individual Variation in Glucocorticoid Plasticity: Considerations and Future Directions

The hypothalamic-pituitary-adrenal (HPA) axis regulates the secretion of glucocorticoids, hormones with diverse roles ranging from regulating daily metabolic demand to coping with sudden perturbations. As a result, glucocorticoids are thought to help vertebrates track their changing environments and coordinate plasticity in diverse phenotypes. While this endocrine system is highly plastic-where one individual can produce multiple phenotypes across varying environmental conditions-little is understood about the degree to which individuals, populations, or species differ in circulating glucocorticoid plasticity. Empirical research quantifying individual variation in glucocorticoid plasticity has increased in recent years, though the multiple complex roles of the HPA-axis make it challenging to generalize the extent to which individual variation in plasticity exists. I provide an overview of current findings on variation in glucocorticoids plasticity, and outline multiple types of glucocorticoid plasticity researchers should consider in future work to advance our understanding of the causes and consequences of individual variation in glucocorticoid plasticity.

Limited mass-independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis).

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass-independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long-term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni- and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass-dependent and mass-independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R=.46) and strongly co-varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass-independent RMR is reduced by 41% to R=.27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass-dependent and mass-independent physiological variation.

A Multiscale Review of Behavioral Variation in Collective Foraging Behavior in Honey Bees.

The emergence of collective behavior from local interactions is a widespread phenomenon in social groups. Previous models of collective behavior have largely overlooked the impact of variation among individuals within the group on collective dynamics. Honey bees (Apis mellifera) provide an excellent model system for exploring the role of individual differences in collective behavior due to their high levels of individual variation and experimental tractability. In this review, we explore the causes and consequences of individual variation in behavior for honey bee foraging across multiple scales of organization. We summarize what is currently known about the genetic, developmental, and neurophysiological causes of individual differences in learning and memory among honey bees, as well as the consequences of this variation for collective foraging behavior and colony fitness. We conclude with suggesting promising future directions for exploration of the genetic and physiological underpinnings of individual differences in behavior in this model system.

Landscape permeability and individual variation in a dispersal-linked gene jointly determine genetic structure in the Glanville fritillary butterfly.

There is now clear evidence that species across a broad range of taxa harbor extensive heritable variation in dispersal. While studies suggest that this variation can facilitate demographic outcomes such as range expansion and invasions, few have considered the consequences of intraspecific variation in dispersal for the maintenance and distribution of genetic variation across fragmented landscapes. Here, we examine how landscape characteristics and individual variation in dispersal combine to predict genetic structure using genomic and spatial data from the Glanville fritillary butterfly. We used linear and latent factor mixed models to identify the landscape features that best predict spatial sorting of alleles in the dispersal‐related gene phosphoglucose isomerase (Pgi). We next used structural equation modeling to test if variation in Pgi mediated gene flow as measured by Fst at putatively neutral loci. In a year when the population was recovering following a large decline, individuals with a genotype associated with greater dispersal ability were found at significantly higher frequencies in populations isolated by water and forest, and these populations showed lower levels of genetic differentiation at neutral loci. These relationships disappeared in the next year when metapopulation density was high, suggesting that the effects of individual variation are context dependent. Together our results highlight that (1) more complex aspects of landscape structure beyond just the configuration of habitat can be important for maintaining spatial variation in dispersal traits and (2) that individual variation in dispersal plays a key role in maintaining genetic variation across fragmented landscapes.

Longitudinal Analysis of Erythrocyte and Plasma Protoporphyrin Levels in Patients with Protoporphyria

Erythropoietic protoporphyria (EPP) and X-linked protoporphyria (XLP) are inherited cutaneous porphyrias resulting from decreased activity of ferrochelatase and gain-of-function mutations of δ-aminolevulinic acid synthase-2, respectively. Both of these protoporphyrias cause increased protoporphyrin levels that cause photosensitivity and may lead to hepatopathy and further increases in erythrocyte and plasma porphyrin levels. We evaluated erythrocyte protoporphyrin and plasma porphyrin levels in all subjects with EPP (83 subjects) or XLP (9 subjects) without evidence of liver disease tested repeatedly at a single laboratory over 25 years. Intersubject variation contributed more than intrasubject variation (78.86% vs 21.14%) to overall variability, and longitudinal variability, estimated by CV, averaged 26%. Erythrocyte total protoporphyrin levels were similar in males and females with EPP (ratio, 0.99; 95% CI, 0.82-1.21; P = 0.96) but were higher in males than females with XLP, although this difference was not statistically significant (ratio, 0.76; 95% CI, 0.43-1.36; P = 0.35). Analysis of 20 subjects from 9 separate families showed significant effects of family compared with effects of individual variation on total variance (50% vs 25%; P < 0.0001). Variation of erythrocyte total protoporphyrin up to 25% is expected in patients with protoporphyria, whereas greater increases might raise concern for protoporphyric hepatopathy.

An intraspecific appraisal of the social intelligence hypothesis.

The prevailing hypotheses for the evolution of cognition focus on either the demands associated with group living (the social intelligence hypothesis (SIH)) or ecological challenges such as finding food. Comparative studies testing these hypotheses have generated highly conflicting results; consequently, our understanding of the drivers of cognitive evolution remains limited. To understand how selection shapes cognition, research must incorporate an intraspecific approach, focusing on the causes and consequences of individual variation in cognition. Here, we review the findings of recent intraspecific cognitive research to investigate the predictions of the SIH. Extensive evidence from our own research on Australian magpies (Cracticus tibicen dorsalis), and a number of other taxa, suggests that individuals in larger social groups exhibit elevated cognitive performance and, in some cases, elevated reproductive fitness. Not only do these findings demonstrate how the social environment has the potential to shape cognitive evolution, but crucially, they demonstrate the importance of considering both genetic and developmental factors when attempting to explain the causes of cognitive variation.This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

Effects of individual variation in length, condition and run‐time on return rates of wild‐reared Atlantic salmon Salmo salar smolts

Groups of wild-reared Atlantic salmon Salmo salar smolts were captured during their seaward migration on a tributary of the River Conon, Scotland, U.K., from 1999 to 2014 and tagged with passive integrated transponders (PIT). Fish that subsequently returned to the river after growing at sea were recorded automatically by a PIT-detector in a fish pass. Return rate was related directly to length and condition and inversely to day of the year that the smolt was tagged. Over years, as the study progressed, there was a significant increase in the proportion of smolts returning after two or more years at sea and no trend in returns of salmon having spent one winter at sea. There was no trend in the date of return of salmon across the study period. Fish that had spent more winters at sea returned earlier in the year.

Baseline glucose level is an individual trait that is negatively associated with lifespan and increases due to adverse environmental conditions during development and adulthood.

High baseline glucose levels are associated with pathologies and shorter lifespan in humans, but little is known about causes and consequences of individual variation in glucose levels in other species. We tested to what extent baseline blood glucose level is a repeatable trait in adult zebra finches, and whether glucose levels were associated with age, manipulated environmental conditions during development (rearing brood size) and adulthood (foraging cost), and lifespan. We found that: (1) repeatability of glucose levels was 30%, both within and between years. (2) Having been reared in a large brood and living with higher foraging costs as adult were independently associated with higher glucose levels. Furthermore, the finding that baseline glucose was low when ambient temperature was high, and foraging costs were low, indicates that glucose is regulated at a lower level when energy turnover is low. (3) Survival probability decreased with increasing baseline glucose. We conclude that baseline glucose is an individual trait negatively associated with survival, and increases due to adverse environmental conditions during development (rearing brood size) and adulthood (foraging cost). Blood glucose may be, therefore, part of the physiological processes linking environmental conditions to lifespan.

Individual size variation reduces spatial variation in abundance of tree community assemblage, not of tree populations.

Research on individual trait variation has gained much attention because of its implication for ecosystem functions and community ecology. The effect of individual variation on population and community abundance (number of individuals) variation remains scarcely tested. Using two established ecological scaling laws (Taylor's law and abundance–size relationship), we derived a new scaling relationship between the individual size variation and spatial variation of abundance. Tested against multi‐plot tree data from Diaoluo Mountain tropical forest in Hainan, China, the new scaling relationship showed that individual size variation reduced the spatial variation of community assemblage abundance, but not of taxon‐specific population abundance. The different responses of community and population to individual variation were reflected by the validity of the abundance–size relationship. We tested and confirmed this scaling framework using two measures of individual tree size: aboveground biomass and diameter at breast height. Using delta method and height‐diameter allometry, we derived the analytic relation of scaling exponents estimated under different individual size measures. In addition, we used multiple regression models to analyze the effect of taxon richness on the relationship between individual size variation and spatial variation of population or community abundance, for taxon‐specific and taxon‐mixed data, respectively. This work offers empirical evidence and a scaling framework for the negative effect of individual trait variation on spatial variation of plant community. It has implications for forest ecosystem and management where the role of individual variation in regulating population or community spatial variation is important but understudied.

Avoiding the misuse of BLUP in behavioural ecology.

Having recognized that variation around the population-level "Golden Mean" of labile traits contains biologically meaningful information, behavioural ecologists have focused increasingly on exploring the causes and consequences of individual variation in behaviour. These are exciting new directions for the field, assisted in no small part by the adoption of mixed-effects modelling techniques that enable the partitioning of among- and within-individual behavioural variation. It has become commonplace to extract predictions of individual random effects from such models for use in subsequent analyses (for example, between a personality trait and other individual traits such as cognition, physiology, or fitness-related measures). However, these predictions are made with large amounts of error that is not carried forward, rendering further tests susceptible to spurious P values from these individual-level point estimates. We briefly summarize the problems with such statistical methods that are used regularly by behavioural ecologists, and highlight the robust solutions that exist within the mixed model framework, providing tutorials to aid in their implementation.

Cortisol and moral decisions among young men: The moderating role of motivation toward closure

Previous research has demonstrated that under stress people make more deontological than utilitarian judgements. We however suggest that the relationship between stress and moral decisions may differ depending on which goals are accessible. In this study we focused on the goal to achieve certainty and individual differences in its importance, expressed as the need for closure. In particular, we examined whether the effects of individual variation in stress levels, measured by cortisol level, on moral decisions depended on individual differences in certainty importance, i.e., the need for closure. Male participants completed the Need for Closure scale and performed a moral decision making task. Saliva samples from these participants were collected. We found that cortisol level was associated with more utilitarian than deontological judgments when achieving certainty was a focal goal (i.e., high need for closure level) but only when ingroup was involved. When certainty reduction is not of such importance (i.e., low need for closure level), groups are not a crucial aid when navigating the social world. In this case, high cortisol levels were associated with more deontological than utilitarian decisions. This was true only for dilemmas in which ingroup was not involved.