Biology subjects

Pemberton, J. M.

Publications and source records attributed to Pemberton, J. M..

At least 19 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↗

bioRxiv2026

Patterns of association between mothers and offspring and their outcomes in a polygynous ungulate

Prolonged association between mothers and their offspring is common in ungulates, with the level of maternal investment likely to play a central role in shaping this trait. Here we examined patterns of association between mothers and offspring over time, the apparent benefits of association to offspring, and costs to mothers. We analyzed 40 years worth of census data from an individually-monitored, food-limited population of red deer (Cervus elaphus) on the Isle of Rum, Scotland. Starting from birth, female calves associated more frequently with their mothers than male calves in their first year. Calves also associated less with their mothers if the mother did not conceive a new calf. Association frequency decreased with mothers age and population density, and survival over the first year was not related to mother-calf association. Yearlings, now in their second year, were more often associated with their mothers if they were female, if there was no subsequent calf (or the subsequent calf died as a neonate), and if they were still being suckled. Increased association between mothers and yearlings was associated with increased survival to adulthood at 28 months, but suckling a yearling did not improve its probability of survival. For individuals that reached maturity, increased association in the yearling year was associated with slightly shorter adult life spans. The level of association between a calf and mother was not associated with the mothers immediate survival or fecundity. Our findings suggest that juveniles born to poor-condition mothers benefit from prolonged association through improved yearling survival.

animal behavior and cognition↗

bioRxiv2026

Fitness costs of parasitism depend on fine-scale density and resource availability in a wild ungulate

Resource competition and parasite exposure both present common density-dependent fitness costs for wild animals. Because launching effective immune responses is costly in terms of resources, parasites fitness costs should be further exacerbated in high-density, resource-depleted areas. To disentangle these relationships, we related density, parasitism, and resource availability to survival and fecundity across lifespan in a long-term study of wild red deer. All fitness measures declined with a combination of parasite count, greater density, and reduced resource availability. Beyond these relationships, as expected, local density and resource scarcity exacerbated survival costs of parasitism in calves, effectively undermining tolerance of infection. However, these synergistic relationships faded in yearlings and then reversed in adults, likely through age-structured selection biases. These findings emphasize that the costs of parasites and resource scarcity can be synergistic and intertwined with density in wild populations, accentuating the value of incorporating resource competition when examining parasite-dependent population regulation.

ecology↗

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↗

bioRxiv2025

Environment dependent benefits of sociality in Soay sheep

An individuals social connections have strong effects on fitness. Despite this, there is pronounced among-individual variation in social behaviour. This variation may be maintained if different types of social connections have environment-dependent fitness benefits, but this has rarely been tested. We applied network analysis to 37 years of social association data in Soay sheep to test this hypothesis. Our results show that both relationship quantity (having many association partners) and relationship quality (having strong associations) are linked with survival. Crucially, the relative importance of relationship quantity and quality depends on overwinter weather, with harsh conditions favouring quantity over quality, likely due to thermoregulatory benefits. Relationship quality, meanwhile, was most beneficial under benign weather conditions, possibly due to enhanced familiarity with conspecifics. These findings advance our understanding of social benefits in fission-fusion societies and show that changing environmental conditions may be an important mechanism maintaining variation in social behaviour in natural populations.

animal behavior and cognition↗

bioRxiv2025

Parasite-mediated inbreeding depression in wild red deer

Inbreeding depression is the reduction in fitness of inbred individuals relative to their more outbred counterparts. Parasitism also reduces fitness and is a route by which inbreeding depression may operate, yet the complete pathway from inbreeding to parasitism to fitness has almost never been documented in the wild. Using high-quality, individual-level data on fitness in juveniles and adult females, longitudinal infection data for three gastrointestinal helminth parasites, and genomic inbreeding coefficients we test for parasite-mediated inbreeding depression in a wild ungulate population (red deer, Cervus elaphus). We found evidence for parasite-mediated inbreeding depression via strongyle nematodes in juvenile survival, independent of direct adverse effects of inbreeding on survival and indirect effects of inbreeding on survival via birth weight. Inbreeding also reduced fitness in reproductive adults by reducing overwinter survival. Our study reveals three independent pathways by which inbreeding depresses fitness and highlights the rarely-studied route of parasitism.

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

Population density drives increased parasitism via greater exposure and reduced resource availability in wild hosts

Exposure to environmental parasites should increase with host population density due to the accumulation of infective parasites in space. However, competition for resources also increases with density, lowering condition and increasing susceptibility, which offers an alternative pathway for density-dependent infection to act. To test how these two processes act independently or together to drive greater parasite counts, we used a long-term study of red deer to examine associations between host density, resource availability, and counts of three common helminth parasites. We found that greater density correlated with reduced resource availability, and while density was positively associated with both strongyle and tissue worm burdens, resource availability was independently and negatively associated with the same burdens, supporting separate roles of density-dependent exposure and susceptibility in driving infection. This study provides evidence that competition for resources is an important driver of infection in higher-density areas, exacerbating the effects of density-dependent increases in exposure.

ecology↗

bioRxiv2024

Evaluating regional heritability mapping methods for identifying QTLs in a wild population of Soay sheep

Regional heritability mapping (RHM) is a method that estimates the heritability of genomic segments that may contain both common and rare variants affecting a complex trait. We compared three RHM methods: SNP-RHM, which uses genomic relationship matrices (GRMs) based on SNP genotypes; Hap-RHM, which uses GRMs based on haplotypes; and SNHap-RHM, which uses both SNP-based and haplotype-based GRMs jointly. We applied these methods to data from a wild population of sheep, analysed eleven polygenic morphometric traits and compared the results with previous genome wide association analyses (GWAS). We found that whilst the inclusion of the regional matrix did not explain significant variation for all regions that were associated with trait variation using GWAS, it did for several regions that were not previously associated with trait variation.

genomics↗

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

Genetic architecture of inbreeding depression may explain its persistence in a population of wild red deer

Inbreeding depression is of major concern in declining populations, but relatively little is known about its genetic architecture in wild populations, such as the degree to which it is composed of large or small effect loci and their distribution throughout the genome. We combine fitness and genomic data from a wild population of red deer to investigate the genomic distribution of inbreeding effects. Inspired by the runs of homozygosity (ROH)-based inbreeding coefficient, FROH, we use chromosome-specific inbreeding coefficients (FROHChr) to explore whether the effect of inbreeding varies between chromosomes. Under the assumption that within an individual the probability of being identical-by-descent is equal across all chromosomes, we used a multi-membership model to estimate the deviation of FROHChr from the average inbreeding effect. This novel approach ensures effect sizes are not overestimated whilst maximising the power of our available dataset containing >35,000 autosomal SNPs. We find that most chromosomes confer a minor reduction in fitness-related traits, which when these effects are summed, results in the observed inbreeding depression in birth weight, survival and lifetime breeding success. However, no chromosomes had a significantly detrimental effect compared to the overall effect of inbreeding. We conclude that in this population, inbreeding depression is the result of multiple mild or moderately deleterious mutations spread across all chromosomes. As predicted by genetic theory these mutations will be inefficiently purged, explaining the persistence of inbreeding depression in this population.

evolutionary biology↗

bioRxiv2023

Investigating pedigree- and SNP-associated components of heritability in a wild population of Soay sheep

Estimates of narrow sense heritability derived from genomic data that contain related individuals may be biased due to the within-family effects such as dominance, epistasis and common environmental factors. However, for many wild populations, removal of related individuals from the data would result in small sample sizes. In 2013, Zaitlen et al. proposed a method to estimate heritability in populations that include close relatives by simultaneously fitting an identity-by-state genomic relatedness matrix (GRM) and an identity-by-descent GRM. The IBD GRM is identical to the IBS GRM, except relatedness estimates below a specified threshold are set to 0. We applied this method to a sample of 8557 wild Soay sheep from St. Kilda, with genotypic information for 419,281 single nucleotide polymorphisms to investigate polygenic and monogenic traits. We also implemented a variant of the model in which the IBD GRM was replaced by a GRM constructed from SNPs with low minor allele frequency to examine whether any additive genetic variance is captured by rare alleles. Each model was compared to an animal model with a single GRM based on all genotyped markers (the IBS GRM) using a log likelihood ratio test. Whilst the inclusion of the IBD GRM did not significantly improve the fit of the model for the monogenic traits, it improved the fit for some of the polygenic traits, suggesting that dominance, epistasis and/or common environment not already captured by the non-genetic random effects fitted in our models may influence these traits.

genetics↗

bioRxiv2023

The carboxyl-terminal sequence of PUMA binds to both anti-apoptotic proteins and membranes.

Anti-apoptotic proteins such as BCL-XL promote cell survival by sequestering pro-apoptotic BCL-2 family members, an activity that frequently contributes to tumorigenesis. Thus, the development of small-molecule inhibitors for anti-apoptotic proteins, termed BH3-mimetics, is revolutionizing how we treat cancer. BH3 mimetics kill cells by displacing sequestered pro-apoptotic proteins to initiate tumor-cell death. Recent evidence has demonstrated that in live cells the BH3-only proteins PUMA and BIM resist displacement by BH3-mimetics, while others like tBID do not. Analysis of the molecular mechanism by which PUMA resists BH3-mimetic mediated displacement from full-length anti-apoptotic proteins (BCL-XL, BCL-2, BCL-W and MCL-1) reveals that both the BH3-motif and a novel binding site within the carboxyl-terminal sequence (CTS) of PUMA contribute to binding. Together these sequences bind to anti-apoptotic proteins, which effectively "double-bolt locks" the proteins to resist BH3-mimetic displacement. The pro-apoptotic protein BIM has also been shown to double-bolt lock to anti-apoptotic proteins however, the novel binding sequence in PUMA is unrelated to that in the CTS of BIM and functions independent of PUMA binding to membranes. Moreover, contrary to previous reports, we find that when exogenously expressed, the CTS of PUMA directs the protein primarily to the endoplasmic reticulum (ER) rather than mitochondria and that residues I175 and P180 within the CTS are required for both ER localization and BH3-mimetic resistance. Understanding how PUMA resists BH3-mimetic displacement will be useful in designing more efficacious small-molecule inhibitors of anti-apoptotic BCL-2 proteins.

cell biology↗

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↗

bioRxiv2023

Selection, recombination and population history effects on runs of homozygosity (ROH) in wild red deer (Cervus elaphus)

The distribution of runs of homozygosity (ROH) may be shaped by a number of interacting processes such as selection, recombination and population history, but little is known about the importance of these mechanisms in shaping ROH in wild populations. We combined an empirical dataset of >3,000 red deer genotyped at >35,000 genome-wide autosomal SNPs and evolutionary simulations to investigate the influence of each of these factors on ROH. We assessed ROH number and location in two populations of red deer (a focal and comparison) to investigate the effect of population history. We investigated the role of recombination using both a physical map and a genetic linkage map to search for ROH. We found differences in ROH distribution between both populations and both map types indicating that population history and local recombination rate have a substantial effect on ROH. Finally, we ran forward genetic simulations with varying population histories, recombination rates and levels of selection, allowing us to further interpret our empirical data. These simulations showed that population history has a greater effect on ROH distribution than either recombination or selection. We further show that selection can cause genomic regions where ROH are common, so called ROH hotspots, only when the effective population size (Ne) is large or selection is particularly strong. In populations having undergone a population bottleneck, genetic drift can outweigh the effect of selection. We show that most ROH hotspots in the Rum population are in line with expectations from neutral simulations, however two ROH hotspots show possible signatures of selection. Overall, we conclude that in this population, genetic drift resulting from a historical population bottleneck is most likely to have resulted in the observed ROH distribution, with selection possibly playing a minor role.

genetics↗

bioRxiv2022

Purifying and balancing selection on embryonic semi-lethal haplotypes in a wild mammal.

Embryonic lethal mutations are arguably the earliest and most severe manifestation of inbreeding depression, but their impact on wild populations is not well understood. Here, we combined genomic, fitness and life-history data from 5,925 wild Soay sheep sampled over nearly three decades to explore the impact of embryonic lethal mutations and their evolutionary dynamics. We searched for haplotypes which in their homozygous state are unusually rare in the offspring of known carrier parents and found three putatively semi-lethal haplotypes with 27-46% fewer homozygous offspring than expected. Two of these haplotypes are decreasing in frequency, and gene-dropping simulations through the pedigree suggest that this is partially due to purifying selection. In contrast, the frequency of the third semi-lethal haplotype remains relatively stable over time. We show that the haplotype could be maintained by balancing selection because it is also associated with increased postnatal survival and body weight and because its cumulative frequency change is lower than in most drift-only simulations. Our study highlights embryonic mutations as a largely neglected contributor to inbreeding depression and provides a rare example of how harmful genetic variation can be maintained through balancing selection in a wild mammal population.

evolutionary biology↗

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↗

bioRxiv2022

Long-term temporal trends in gastrointestinal parasite infection in wild Soay sheep

Monitoring the prevalence and abundance of parasites over time is important for addressing their potential impact on host life-histories, immunological profiles, and their influence as a selective force. Only long-term ecological studies have the potential to shed light on both the temporal trends in infection prevalence and abundance and the drivers of such trends, because of their ability to dissect drivers that may be confounded over shorter time scales. Despite this, only a relatively small number of such studies exist. Here, we analysed changes in the prevalence and abundance of gastrointestinal parasites in the wild Soay sheep population of St Kilda across 31 years. The host population density has increased across the study, and population density is known to increase parasite transmission, but we found that density and year explained temporal variation in parasite prevalence and abundance independently. Prevalence of both strongyle nematodes and coccidian microparasites increased during the study, and this effect varied between lambs, yearlings and adults. Meanwhile, abundance of strongyles was more strongly linked to host density than to temporal (yearly) dynamics, while abundance of coccidia showed a strong temporal trend without any influence of density. Strikingly, coccidian abundance increased threefold across the course of the study in lambs, while increases in yearlings and adults were negligible. Our decades-long, intensive, individual-based study will enable the role of environmental change and selection pressures in driving these dynamics to be determined, potentially providing unparalleled insight into the drivers of temporal variation in parasite dynamics in the wild. Key findingsO_LIWe studied temporal trends in gastrointestinal parasites of wild sheep over 31 years C_LIO_LIYear and host population density explained temporal variation in parasites independently C_LIO_LIPrevalence of both strongyle nematodes and coccidia varied across the study period C_LIO_LIAbundance of strongyles was more closely linked to host density than year C_LIO_LIAbundance of coccidia increased threefold over time in lambs, but did not vary in adults C_LI

ecology↗