Josephine M. Pemberton’s research while affiliated with University of Edinburgh and other places

An individual's 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.

Early-life adversity influences adult fitness across vertebrate species. In polygynous systems with intense intrasexual competition, males may be more sensitive to conditions experienced during development. However, the importance of different aspects of the early-life environment and how their effects differ between the sexes remains poorly understood. Here, we used a long-term study of wild Soay sheep to characterize the early-life environment in terms of weather, infection risk, resource competition and maternal investment, and test the hypothesis that males are more vulnerable to early adversity. Birth weight, reflective of maternal investment and conditions during gestation, positively predicted lifetime breeding success in both sexes, suggesting a classic ‘silver spoon’ effect, though the effects were stronger in males. Males that experienced increased resource competition in their first year had lower lifetime breeding success, suggesting lasting negative consequences of nutritional stress, but there was no association in females. By contrast, challenging weather in the first winter of life was associated with stronger viability selection, 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, demonstrating distinct aspects of the early environment may shape fitness in different and sex-specific ways.

Background T-helper (Th) cells co-ordinate immune responses to ensure that infections with diverse parasites are controlled effectively. Helminth parasites such as gastro-intestinal nematodes (GIN) are generally associated with T-helper type 2 (Th2) responses, while intracellular parasites are associated with Th1 responses. Although laboratory models have reported that Th1 and Th2 can be antagonistic, this has been challenged by studies of natural infections. Methods Between 2019 and 2022 we completed 759 captures of 538 wild Soay sheep (1-4 captures per animal) and monitored body weight, parasite egg counts, Th phenotypes, cytokines and GIN-specific antibodies. Results While different Th cell counts, cytokines and antibody isotypes were generally positively correlated with each other, no strong positive associations were observed between these measurements. Cell counts had low repeatability (among-individual variation) across four years, while antibody levels were highly repeatable. The Th1 and Th2 cytokines IFN-γ and IL-4 were moderately repeatable and were positively correlated at both the between- and within-individual levels independent of body condition or parasite exposure. IL-4 was negatively associated with GIN faecal egg count, while IFN-γ was negatively associated with coccidian faecal oocyst count, suggesting that these cytokines reflect resistance to these parasites. None of our immune markers were strongly associated with lamb survival. Conclusions Our results provide insights into how different aspects of immune function interact to produce effective responses to complex infections but suggest longer term data collection is required to address the causes of these interactions and to detect fitness consequences of variation in T cell phenotypes under natural conditions.

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.

Sex chromosomes differ in their inheritance properties from autosomes, and hence may encode complementary information about past demographic events. We compiled and analysed a range-wide resequencing dataset of the red deer (Cervus elaphus), one of the few Eurasian herbivores of the Late Pleistocene megafauna still found throughout much of its historic range. Our analyses of 144 whole genomes reveal striking discrepancies between the population clusters suggested by autosomal and X-chromosomal data. We postulate that the genetic legacy of Late Glacial population structure is better captured and preserved by the X chromosome than by autosomes, for two reasons. First, X chromosomes have a lower Ne and hence lose genetic variation faster during isolation in glacial refugia, causing increased population differentiation. Second, following postglacial recolonisation and secondary contact, immigrant males pass on their X chromosomes to female offspring only, which effectively halves the migration rate when gene flow is male-mediated. Our study illustrates how a comparison between autosomal and sex chromosomal phylogeographic signals unravels past demographic processes which otherwise would remain hidden.

Environmental stress can exacerbate inbreeding depression by amplifying differences between inbred and outbred individuals. In wild populations, where the environment is often unpredictable and stress can be highly detrimental, the interplay between inbreeding depression and environmental variation is potentially important. Here, we investigate variation in inbreeding level, fitness and strength of inbreeding depression across a fine-scale geographic area (~12 km2) in an individually monitored population of red deer (Cervus elaphus). We show that northern regions of the study area have lower birth weights, lower juvenile survival rates, and higher inbreeding coefficients. Such fine-scale differences in inbreeding coefficients could be caused by the mating system of red deer combined with female density variation. We then tested for an inbreeding depression-by-environment interaction (ID × E) in birth weight and juvenile survival, by fitting an interaction term between the inbreeding coefficient and geographic location. We find that inbreeding depression in juvenile survival is stronger in the harsher northern regions, indicating the presence of ID × E. We also highlight that the ability to infer ID × E is affected by the variation in inbreeding within each geographic region. Therefore, for future studies on ID × E in wild populations, we recommend first assessing whether inbreeding and traits vary spatially or temporally. Overall, this is one of only a handful of studies to find evidence for ID × E in a wild population—despite its prevalence in experimental systems—likely due to intense data demands or insufficient variation in environmental stress or inbreeding coefficients.

As animals age, they exhibit a suite of phenotypic changes, often including reductions in movement and social behaviour (‘behavioural ageing’). By altering an individual’s exposure to parasites, behavioural ageing may influence infection status trajectories over the lifespan. However, these processes could be confounded by age-related changes in other phenotypic traits, or by selective disappearance of certain individuals owing to parasite-induced mortality. Here, we uncover contrasting age-related patterns of infection across three helminth parasites in wild adult female 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, and lungworm (Dictyocaulus) counts did not change. These relationships could not be explained by socio-spatial behaviours, spatial structuring, or selective disappearance, suggesting behavioural ageing is unlikely to be responsible for driving age trends. Instead, social connectedness and strongyle infection were positively correlated, such that direct age–infection trends were directly contrasted with the effects implied by previously documented behavioural ageing. This suggests that behavioural ageing may reduce parasite exposure, potentially countering other age-related changes. These findings demonstrate that different parasites can show contrasting age trajectories depending on diverse intrinsic and extrinsic factors, and that behaviour’s role in these processes is likely to be complex and multidirectional. This article is part of the discussion meeting issue ‘Understanding age and society using natural populations’.

Climate change‐driven impacts on vegetation productivity have been shown to drive mammalian herbivore population dynamics in Arctic and alpine environments. However, there is less evidence for temperate systems. To address this, we examined the contribution of increasing plant biomass in different vegetation communities (measured by NDVI, normalised difference vegetation index) and winter weather on the observed long‐term upward trend in the population of the Soay sheep of Hirta, St Kilda, UK. We found that biomass had increased in all vegetation communities present and increased the fastest in vegetation types preferred by the sheep. Specifically, those communities with high specific leaf area and Ellenberg's N, low leaf dry matter content. Peak summer NDVI and either winter average wind speed or winter North Atlantic Oscillation data added to the variance explained by a simple density dependence model of yearly sheep population growth rates. The highest explanatory power was found for preferred vegetation types including maritime cliff communities dominated by Plantago species, but also for both inaccessible ( Rumex acetosa ‐dominated) or unpreferred ( Eriophorum vaginatum‐ or Sphagnum ‐dominated) communities where seasonal variation more closely reflects productivity due to minimal grazing. Although the climate is getting windier and wetter, it is also getting warmer allowing increased plant productivity and this appears to be behind the long‐term increases in the Soay sheep population. Our study indicates that analysing key vegetation communities may reveal these links better than using landscape‐level averages, and that oceanic‐temperate systems may show similar climate‐driven herbivore population trends to those reported in Arctic and alpine systems.

While senescence is a common occurrence in wild populations, not all traits decline with age simultaneously and some do not show any senes- cence. A lack of senescence in secondary sexual traits is thought to be due to their importance for reproductive success. However, if reproduc- tive success senesces, why would secondary sexual traits apparently not senesce? Here we explored this question in a wild population of red deer (Cervus elaphus) using antler form (number of points), a secondary sexual trait which shows little senescence, despite the occurrence of reproductive senescence. In line with expectations for traits that senesce, genetic vari- ance in antler form increased with age and selection weakened with age. Therefore, there was no indication that stronger selection on individu- als that survived to older ages was countering the dilution of selection due to fewer individuals being alive. Furthermore, the effect of selec- tive disappearance masking a slight decline in antler form in the oldest years was small. Interestingly, although genetic variance and positive se- lection of antler form were found, there was no evidence of a response to selection, supporting a genetic decoupling of antler senescence and re- productive senescence. Finally, a positive genetic covariance in antler form among age classes provides a possible explanation for the the lack of senescence. These findings suggest that antler form is under a genetic constraint that prevents it from senescing, providing an interesting evolu- tionary explanation for negligible senescence in a secondary sexual trait, and consequently, the existence of asynchrony in senescence among traits within populations.