Biology subjects

Nussey, D. H.

Publications and source records attributed to Nussey, D. H..

17 recordsLinked to original sources

bioRxiv2026

No evidence sex-specific senescence varies with resource competition in Soay sheep

Demographic senescence, the age-related decline in survival and reproduction, is widespread. Older individuals, and particularly males in polygynous systems, are expected to be disproportionately vulnerable to environmental stressors due to physiological decline and high reproductive costs. However, studies testing if harsh conditions exacerbate senescence, and whether this effect is sex-dependent, remain limited in wild populations. Using 40 years of data from wild Soay sheep (Ovis aries) on St Kilda, Scotland, we tested whether increased resource competition (indexed by population density) accelerates demographic senescence, and if late-life environmental sensitivity is male-biased. High densities consistently suppressed overall adult performance, making individuals less likely to survive, breed, or rear high-quality offspring under more intense competition. Although survival and reproductive traits exhibited clear senescence, increased population density did not accelerate late-life declines in any trait. Rates of decline with age were unaffected by density and did not differ between the sexes. Our results challenge the assumption that older individuals and males are inherently more vulnerable to harsh conditions, suggesting physiological or behavioural buffering may maintain late-life resilience against resource limitation in some systems.

evolutionary biology↗

bioRxiv2025

Plasma insulin-like growth-factor 1 (IGF-1) concentrations predict early life-history traits in a wild mammal

O_LIThe hormone insulin-like growth factor 1 (IGF-1) is a key player in the insulin/IGF-1 signaling (IIS) pathway. Extensive biogerontological research demonstrates that this evolutionarily conserved nutrient-sensing pathway plays a causal role in the regulation of growth, reproduction and longevity under laboratory conditions. However, its potential role as a mediator of adaptive life-history variation in highly variable natural environments remains unclear. C_LIO_LIWe measured IGF-1 concentrations in blood samples from approximately four-month-old wild Soay sheep lambs (n=669), collected over nine summers. We tested whether IGF-1 (i) was positively correlated with proxies of resource availability, (ii) was associated with morphological traits measured concurrently, and (iii) predicted subsequent fitness-related traits. C_LIO_LIPlasma IGF-1 concentrations were higher in males compared to females, and positively correlated with measures of resource availability in both sexes. IGF-1 was lower in years of high population density when per capita food availability was reduced; in twin lambs who have fewer available resources compared to singletons; and in lambs born to young and old mothers, who have poor maternal provisioning compared to mothers of intermediate age. C_LIO_LIHigher IGF-1 levels in summer were correlated with higher body mass, faster post-natal somatic growth and increased skeletal size, measured at the same time. These associations were independent of our proxies of resource availability. C_LIO_LILambs with higher summer IGF-1 were more likely to survive their first winter and reproduce the following spring. The association between IGF-1 and reproduction was independent of our resource availability proxies, whereas the association with first-winter survival was not. The association between summer IGF-1 and reproduction was mediated by positive associations with summer body mass. C_LIO_LIOur study reveals population-level phenotypic plasticity in circulating IGF-1, also finding IGF-1 to be positively associated with key morphological traits and positively predict fitness traits in early life. These findings highlight IGF-1 as a candidate physiological mechanism underpinning plastic responses to variation in food availability and influencing life-history traits in a wild mammal. C_LI

ecology↗

bioRxiv2024

Sex-specific effects of early-life adversity on adult fitness in a wild mammal

Early-life adversity influences adult fitness across a range of vertebrates. In polygynous systems with intense intrasexual competition, males may be more sensitive to conditions experienced during growth and development. However, the relative importance of different aspects of the early environment and how their effects differ between the sexes remain poorly understood. Here, we used a long-term study of wild Soay sheep to characterise the early-life environment in terms of weather, infection, resource competition and maternal investment, and test the hypothesis that males are more vulnerable to early adversity than females. Birth weight positively predicted lifetime breeding success in both sexes, suggesting a classic silver spoon effect, though the effects were stronger in males. Males experiencing high population densities in their first year had lower lifetime breeding success suggesting lasting negative consequences of nutritional stress, but there was no association in females. In contrast, challenging weather in the first winter of life appeared to act as a selective filter, with males surviving these harsh conditions having higher adult fitness. Our findings further evidence the important long-term fitness consequences of early-life adversity in wild vertebrates, highlighting that different aspects of the early environment may shape later fitness in different and sex-specific ways.

evolutionary biology↗

bioRxiv2024

Local and global density have distinct and parasite-dependent effects on infection in wild sheep

High density should drive greater parasite exposure. However, evidence linking density with infection generally uses density proxies, rather than of individuals per space within a continuous population. We used a long-term study of wild sheep to link within-population spatiotemporal variation in host density with individual parasite counts. Although four parasites exhibited strong positive relationships with local density, these relationships were mostly restricted to juveniles and faded in adults. Further, one ectoparasite showed strong negative relationships across all age classes. In contrast, population size - a measure of global density - had limited explanatory power, and its effects did not remove those of spatial density, but were complementary. These results indicate that local and global density can exhibit diverse and contrasting effects on infection within populations. Spatial measures of within-population local density may provide substantial additional insight to temporal metrics based on population size, and investigating them more widely could be highly revealing.

ecology↗

bioRxiv2023

Age specific impacts of vegetation functional traits on gastro-intestinal nematode parasite burdens in a large herbivore

O_LIGastro-intestinal nematode (GIN) parasites play an important role in the ecological dynamics of many animal populations. Recent studies suggest fine-scale spatial variation in GIN infection dynamics are important in wildlife systems, but the environmental drivers underlying this variation remain poorly understood. C_LIO_LIWe used data from over two decades of GIN parasite egg counts, host space use, and spatial vegetation data from a long-term study of Soay sheep on St Kilda to test how spatial autocorrelation and vegetation in an individuals home range predict parasite burden across three age groups. We developed a novel approach to quantify the plant functional traits present in a home range to describe the quality of vegetation present. C_LIO_LIEffects of space and vegetation varied between age classes. In immature lambs, strongyle parasite faecal egg counts (FEC) were spatially structured, being highest in the north and south of our study area. Independent of host body weight and spatial autocorrelation, plant functional traits predicted parasite egg counts. Higher egg counts were associated with more digestible and preferred plant functional traits, suggesting the association could be driven by host density and habitat preference. C_LIO_LIIn contrast, we found no evidence that parasite FEC were related to plant functional traits in the host home range in yearlings or adult sheep. Adult FEC were spatially structured, with highest burdens in the north-east of our study area, while yearling FEC showed no evidence of spatial structuring. C_LIO_LIOur findings support the importance of fine-scale environmental variation for wildlife disease ecology and provides new evidence that such effects may vary across demographic groups within a population. Parasite burdens in immature individuals appear more readily influenced by fine-scale spatial variation in the environment, highlighting the importance of such heterogeneity for our understanding of wildlife epidemiology and health. C_LI

ecology↗

bioRxiv2022

Different helminth parasites show contrasting relationships with age in a wild ungulate

As animals age they often exhibit substantial physiological and behavioural changes that can drive changes in infection status over the lifespan. Generally, immunosenescence is expected to lead to greater infection in older individuals, but this process could be confounded or counteracted by changes in behaviour, selective disappearance of certain individuals, or a range of immune processes. Here, we uncover contrasting age-related patterns of infection across three different helminth parasites in wild adult red deer (Cervus elaphus). Counts of strongyle nematodes (order: Strongylida) increased with age, while counts of liver fluke (Fasciola hepatica) and tissue worm (Elaphostrongylus cervi) decreased. These relationships could not be explained by selective disappearance of certain individuals or changes in behaviour, suggesting that immune changes could be responsible. Additionally, we found a positive relationship between social connectedness and strongyle infection, implying that previously documented age-related decreases in social behaviour may minimise exposure, reducing the negative effects of immunosenescence. These findings demonstrate that burdens of different parasites can show contrasting changes over an individuals lifespan depending on a complex suite of intrinsic and extrinsic factors.

ecology↗

bioRxiv2021

Ageing red deer alter their spatial behaviour and become less social

Social relationships are important to many aspects of animals lives, and an individuals connections may change over the course of their lifespan. Currently, it is unclear whether social connectedness declines within individuals as they age, and what the underlying mechanisms might be, so the role of age in structuring animal social systems remains unresolved, particularly in non-primates. Here, we describe senescent declines in social connectedness using 43 years of data in a wild, individually monitored population of a long-lived mammal (European red deer, Cervus elaphus). Applying a series of spatial and social network analyses, we demonstrate that these declines occur due to within-individual changes in social behaviour, with correlated changes in spatial behaviour (smaller home ranges and movements to lower-density, lower-quality areas). These findings demonstrate that within-individual socio-spatial behavioural changes can lead older animals in fission-fusion societies to become less socially connected, shedding light on the ecological and evolutionary processes structuring wild animal populations.

ecology↗

bioRxiv2021

Functionally distinct T-helper cell phenotypes predict resistance to different types of parasites in a wild mammal

O_LIThe adaptive immune system is critical to an effective, long-lasting ability to respond to infection in vertebrates and T-helper (Th) cells play a key role in orchestrating the adaptive immune response. Laboratory studies show that functionally distinct Th responses provide protection against different kinds of parasites (i.e., Th1 responses against microparasites and Th2 against macroparasites). C_LIO_LINatural populations must deal with challenges from a wide range of infectious agents and co-infection with different types of parasite is the norm, so different Th responses are likely to play an important and dynamic role in maintaining host health and fitness. However, the relationship between T helper immune phenotypes and infection with different types of parasites remains poorly understood in wild animals. C_LIO_LIIn this study, we characterised variation in functionally distinct Th responses (Th1, Th2, Th17 and regulatory responses) in a wild population of Soay sheep using flow cytometry to detect Th-subset specific transcription factors, and ex vivo lymphocyte stimulation to quantify release of Th-associated cytokines. We specifically tested the prediction that raised Th1 and Th2 responses should predict reduced apicomplexan (coccidian) and helminth (nematode) parasite burdens, respectively. C_LIO_LICell counts of different Th subsets measured by flow cytometry did not vary with age or sex. However, all measures of Th-associated ex vivo cytokine production increased with age, and Th17- and regulatory Th-associated cytokine production increased more rapidly with age in males than females. C_LIO_LIIndependent of age and sex, Th2-associated immune measures negatively predicted gastro-intestinal strongyle nematode faecal egg count, while production of the Th1-associated cytokine IFN-{gamma} negatively predicted coccidian faecal oocyst count. C_LIO_LIOur results provide important support from outside the laboratory that Th1 and Th2 responses confer resistance to different kinds of parasites (micro- and macro-parasites, respectively). They also add to mounting evidence from wild populations that Th1/Th2 trade-offs often observed in controlled laboratory experiments may not readily translate to more complex natural systems. C_LIO_LIOur study illustrates that harnessing more specific reagents and tools from laboratory immunology has the potential to illuminate our understanding of epidemiology and host-parasite co-evolution in the wild. C_LI

ecology↗

bioRxiv2021

Seasonal dynamics and repeatability of gastrointestinal parasite burdens in wild Soay sheep

Seasonality is a ubiquitous feature of wildlife disease ecology, but is determined by a complex interplay of environmental, parasitological and host factors. Gastrointestinal parasites often exhibit strong seasonal dynamics in wild vertebrate populations due to, for example, environmental influences on free-living or vectored life stages, and variation in the physiological and immune status of hosts across their annual cycle. At the same time, wild populations are typically infected with multiple parasites. The seasonal dynamics of co-infecting parasites may differ depending on age and reproductive status, and associations among parasites may be driven by short-term within-individual changes or longer-term interactions that are consistent among hosts. Here, we used faecal samples and egg counts collected repeatedly from individually marked and monitored wild Soay sheep that were part of a long-term study to investigate seasonal dynamics of six gastrointestinal parasite groups (strongyle nematodes, coccidian protozoa, Capillaria, Strongyloides, Nematodirus, and Moniezia). Prevalence and abundance generally tended to be higher spring and summer, and burdens were higher in lambs than adults. Within the highly prevalent strongyle nematode group, we found differences in seasonality of egg counts depending on adult reproductive status. Reproductive ewes had increased counts in spring around the time of birth followed by a drop in abundance in summer, while barren ewes showed little evidence of seasonality. Males showed a sustained rise in egg counts through spring and summer, and sex differences were only strongly apparent in summer. In contrast, in similarly prevalent coccidia we found a peak in faecal oocyst counts in spring but no differences in seasonality among males, barren and pregnant ewes. Using multivariate mixed-effects models, we went on to show that both strongyle and coccidia counts are moderately repeatable across seasons among individuals. We further show that apparent positive correlation between strongyle and coccidia counts was driven by short-term within-individual changes in both parasite burdens rather than long-term among-individual covariation. Overall, our results demonstrate that seasonality varies across demographic and parasite groups and highlight the value of investigating fluctuating susceptibility and exposure over time for understanding epidemiology of a population.

ecology↗

bioRxiv2020

A mixed model approach for estimating drivers of microbiota community composition and differential taxonomic abundance

O_LINext-generation sequencing (NGS) and meta-barcoding approaches have revolutionized understanding of within-host communities, such as the gut microbiome, in humans and laboratory animals. The application of such approaches in wild animal populations is growing, but there is a disconnect between the widely-applied generalised linear mixed model (GLMM) approaches commonly used to study phenotypic variation and the statistical toolkit from community ecology which is typically applied to meta-barcoding data. C_LIO_LIHere, we describe and illustrate a novel GLMM-based approach for analysing the taxon-specific sequence read counts derived from standard meta-barcoding data. This approach allows us to decompose the contribution of different drivers of variation in community structure (e.g. year, season, individual host), via interaction terms in the random effects structure of the model. We also show how these models can be used to determine the degree to which specific taxa or taxonomic groups are responsible for variance attributed to different drivers. C_LIO_LITo illustrate this approach, we applied it to two cross-sectional meta-barcoding data sets from the Soay Sheep population of St. Kilda. The GLMM approach yielded results that were in agreement with more classical approaches from community ecology, showing that variation the gut microbiota community in these sheep was better explained by age group than by season. We were able to quantify the contributions of different sources of variation to community structure, and also to drill down into the model predictions to show that the age effects we observed were principally due to increases in taxa of the phyla Bacteroidetes and declines in taxa of the phyla Firmicutes. C_LIO_LIOur proposed models offer a powerful new approach to understanding the drivers of variation in estimates of community structure derived from meta-barcoding data. We discuss how our approach could be readily adapted to allow researchers to estimate that contribution of host genotype, environment, and microbial/parasite phylogeny to observed community structure, and thus provide a powerful means to answer emerging questions surrounding the ecological and evolutionary roles of within-host communities. C_LI

evolutionary biology↗

bioRxiv2020

Vitamin D status is heritable and under environment-dependent selection in the wild.

Vitamin D has a well-established role in skeletal health and is increasingly linked to chronic disease and mortality in humans and companion animals. Despite the clear significance of vitamin D for health and obvious implications for fitness under natural conditions, no longitudinal study has tested whether the circulating concentration of vitamin D is under natural selection in the wild. Here, we show that concentrations of dietary-derived vitamin D2 and endogenously-produced vitamin D3 metabolites are heritable and largely polygenic in a wild population of Soay sheep (Ovis aries). Vitamin D2 status was positively associated with female adult survival, and vitamin D3 status predicted female fecundity in particular, good environment years. Our study provides evidence that vitamin D status has the potential to respond to selection, as well as new insights into how vitamin D metabolism is associated with fitness in the wild.

evolutionary biology↗

bioRxiv2020

Life-long telomere attrition predicts health and lifespan in a large mammal

Telomere length measured in blood cells is predictive of subsequent adult health and survival across a range of vertebrate species. However, we currently do not know whether such associations result from among-individual differences in telomere length determined genetically or by environmental factors early in life, or from differences in the rate of telomere attrition over the course of life. Here, we measured relative leukocyte telomere length (RLTL) multiple times across the entire lifespan of dairy cattle in a research population that is closely monitored for health and milk production and where individuals are only culled in response to health issues and less due to poor milk production than on purely commercial farms. Our results clearly show that the average amount of telomere attrition over an individuals life, not their average or early life telomere length predicted when an individual was culled. Within-individual telomere length attrition could reflect environmental or physiological insults which may accumulate to predict individual health-span. We also show that animals with more telomere attrition in their first year of life were culled at a younger age, indicating that early life stressors may have a prolonged effect on adult life.

evolutionary biology↗

bioRxiv2020

Spatial point locations explain a range of social network positions in a wild ungulate

The structure of wild animal social systems depends on a complex combination of intrinsic and extrinsic drivers. Population structuring and spatial behaviour are key determinants of individuals observed social behaviour, but quantifying these spatial components alongside multiple other drivers remains difficult due to data scarcity and analytical complexity. We used a 43-year dataset detailing a wild red deer population to investigate how individuals spatial behaviours drive social network positioning, while simultaneously assessing other potential contributing factors. Using Integrated Nested Laplace Approximation (INLA) multi-matrix animal models, we demonstrate that social network positions are shaped by two-dimensional landscape locations, pairwise space sharing, individual range size, and spatial and temporal variation in population density, alongside smaller but detectable impacts of a selection of individual-level phenotypic traits. These results indicate strong, multifaceted spatiotemporal structuring in this society, emphasising the importance of considering multiple spatial components when investigating the causes and consequences of sociality. Authorship StatementGFA conceived the study, analysed the data, and wrote the manuscript, advised by JAF. AM and SM collected the data. JAF, JMP, THCB, and DN commented on the manuscript. Data Accessibility StatementThe code used here is available at https://github.com/gfalbery/Spocial_Deer. On acceptance, the data will be uploaded to the same repo, which will be archived on Zenodo.

ecology↗

bioRxiv2019

Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal

Reproduction in wild animals can divert limited resources away from immune defence, resulting in increased parasite burdens. A longstanding prediction of life history theory states that these parasites can harm the reproductive individual, reducing its subsequent fitness and producing reproduction-fitness tradeoffs. Here, we examined associations among reproductive allocation, immunity, parasitism, and subsequent fitness in a wild population of individually identified red deer (Cervus elaphus). Using path analysis, we investigated whether costs of lactation for downstream survival and fecundity were mediated by changes in strongyle nematode count and mucosal antibody levels. Lactating females exhibited increased parasite counts, which were in turn associated with substantially decreased fitness in the following year in terms of overwinter survival, fecundity, subsequent calf weight, and parturition date. This study offers observational evidence for parasite regulation of multiple life history tradeoffs, supporting the role of parasites as an important mediating factor in wild mammal populations.

ecology↗

bioRxiv2019

The genetic architecture of helminth-specific immune responses in a wild population of Soay sheep (Ovis aries)

Host-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural populations. Variation in immune responses to infection is likely to shape the outcome of these interactions, with important consequences for the fitness of both host and parasite. However, little is known about how genetic variation contributes to variation in immune responses under natural conditions. Here, we examine the genetic architecture of variation in immune traits in the Soay sheep of St Kilda, an unmanaged population of sheep infected with strongyle gastrointestinal nematodes. We assayed IgA, IgE and IgG antibodies against the prevalent nematode Teladorsagia circumcincta in the blood plasma of > 3,000 sheep collected over 26 years. Antibody levels were significantly heritable, ranging from 0.21 to 0.39 in lambs and from 0.23 to 0.57 in adults. IgA levels were strongly associated with a region on chromosome 24 explaining 21.1% and 24.5% of heritable variation in lambs and adults, respectively; this region was adjacent to two candidate loci, the Class II Major Histocompatibility Complex Transactivator (CIITA) and C-Type Lectin Domain Containing 16A (CLEC16A). Lamb IgA levels were also associated with the immunoglobulin heavy constant loci (IGH) complex on chromosome 18. Adult IgE levels and lamb IgG levels were associated with the major histocompatibility complex (MHC) on chromosome 20. This study provides evidence of high heritability of a complex immunological trait under natural conditions and provides the first evidence from a genome-wide study that large effect genes located outside the MHC region exist for immune traits in the wild.\n\nAuthor summaryHost-parasite interactions are powerful drivers of evolutionary and ecological dynamics in natural populations. Variation in immune responses to infection shapes the outcome of these interactions, with important consequences for the ability of the host and parasite to survive and reproduce. However, little is known about how much genes contribute to variation in immune responses under natural conditions. Our study investigates the genetic architecture of variation in three antibody types, IgA, IgE and IgG in a wild population of Soay sheep on the St Kilda archipelago in North-West Scotland. Using data collected over 26 years, we show that antibody levels have a heritable basis in lambs and adults and are stable over lifetime of individuals. We also identify several genomic regions with large effects on immune responses. Our study offers the first insights into the genetic control of immunity in a wild population, which is essential to understand how immune profiles vary in challenging natural conditions and how natural selection maintains genetic variation in complex immune traits.

genetics↗

bioRxiv2018

The fine-scale landscape of immunity and parasitism in a wild ungulate population

Spatial heterogeneity in parasite susceptibility and exposure is a common source of confounding variation in disease ecology studies. However, it is not known whether spatial autocorrelation acts on immunity in particular at small scales, within wild animal populations, and whether this predicts spatial patterns in infection. Here we used a well-mixed wild population of individually recognised red deer (Cervus elaphus) inhabiting a heterogeneous landscape to investigate fine-scale spatial patterns of immunity and parasitism. We noninvasively collected 842 faecal samples from 141 females with known ranging behaviour over two years. We quantified total and helminth-specific mucosal antibodies and counted propagules of three gastrointestinal helminth taxa. These data were analysed with linear mixed models using the Integrated Nested Laplace Approximation (INLA), using a Stochastic Partial Differentiation Equation approach (SPDE) to control for and quantify spatial autocorrelation. We also investigated whether spatial patterns of immunity and parasitism changed seasonally. We discovered substantial spatial heterogeneity in general and helminth-specific antibody levels and parasitism with two helminth taxa, all of which exhibited contrasting seasonal variation in their spatial patterns. Notably, strongyle nematode intensity did not align with density hotspots, while Fasciola hepatica intensity appeared to be strongly influenced by the presence of wet grazing. In addition, antibody hotspots did not correlate with distributions of any parasites. Our results suggest spatial heterogeneity may be an important factor affecting immunity and parasitism in a wide range of study systems. We discuss these findings with regards to the design of sampling regimes and public health interventions, and suggest that disease ecology studies investigate spatial heterogeneity more regularly to enhance their results, even when examining small geographic areas.

ecology↗

bioRxiv2018

Reproduction has different costs for immunity and parasitism in a wild mammal

1. Life history theory predicts that reproductive investment draws resources away from immunity, resulting in increased parasitism. However, studies of reproductive tradeoffs rarely examine multiple measures of reproduction, immunity, and parasitism. It is therefore unclear whether the immune costs of reproductive traits correlate with their resource costs, and whether increased parasitism emerges from weaker immunity.\n\n2. We examined these relationships in wild female red deer (Cervus elaphus) with variable reproductive investment and longitudinal data on mucosal antibody levels and helminth parasitism. We noninvasively collected faecal samples, counting propagules of strongyle nematodes (order: Strongylida), the common liver fluke Fasciola hepatica and the red deer tissue nematode Elaphostrongylus cervi. We also quantified both total and anti-strongyle mucosal IgA to measure general and specific immune investment.\n\n3. Contrary to our predictions, we found that gestation was associated with decreased total IgA but with no increase in parasitism. Meanwhile, the considerable resource demand of lactation had no further immune cost but was associated with higher counts of strongyle nematodes and Elaphostrongylus cervi. These contrasting costs arose despite a negative correlation between antibodies and strongyle count, which implied that IgA was indicative of protective immunity.\n\n4. Our findings suggest that processes other than classical resource allocation tradeoffs are involved in mediating observed relationships between reproduction, immunity, and parasitism in wild mammals. In particular, reproduction-immunity tradeoffs may result from hormonal regulation or maternal antibody transfer, with parasitism increasing as a result of increased exposure arising from resource acquisition constraints. We advocate careful consideration of resource-independent mechanistic links and measurement of both immunity and parasitism when investigating reproductive costs.

ecology↗