Biology subjects

Pemberton, J. M.

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

At least 37 records · Page 2Linked to original sources

bioRxiv2022

The impact of SNP density on quantitative genetic analyses of body size traits in a wild population of Soay sheep

Understanding the genetic architecture underpinning quantitative traits in wild populations is pivotal to understanding the processes behind trait evolution. The animal model is a popular method for estimating quantitative genetic parameters such as heritability and genetic correlation and involves fitting an estimate of relatedness between individuals in the study population. Genotypes at genome-wide markers can be used to estimate relatedness; however, relatedness estimates vary with marker density, potentially affecting results. Increasing density of markers is also expected to increase the power to detect quantitative trait loci (QTL). In order to understand how the density of genetic markers affects the results of quantitative genetic analyses, we estimated heritability and performed genome-wide association studies (GWAS) on five body size traits in an unmanaged population of Soay sheep using two different SNP densities: a dataset of 37,037 genotyped SNPs, and an imputed dataset of 417,373 SNPs. Heritability estimates did not differ between the two SNP densities, but the high-density imputed SNP dataset revealed four new SNP-trait associations that were not found with the lower density dataset, as well as confirming all previously-found QTL. We also demonstrated that fitting fixed and random effects in the same step as performing GWAS is a more powerful approach than pre-correcting for covariates in a separate model.

genomics↗

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

Admixture mapping reveals loci for carcass mass in red deer x sika hybrids in Kintyre, Scotland

We deployed admixture mapping on a sample of 386 deer from a hybrid swarm between native red deer (Cervus elaphus) and introduced Japanese sika (Cervus nippon) sampled in Kintyre, Scotland to search for Quantitative Trait Loci (QTL) underpinning phenotypic differences between the species. These two species are highly diverged genetically (Fst between pure species, based on 50K SNPs, = 0.532) and phenotypically: pure red have on average twice the carcass mass of pure sika in our sample (38.7kg vs 19.1 kg). After controlling for sex, age and population genetic structure we found ten autosomal genomic locations with QTL for carcass mass. Effect sizes ranged from 0.191 to 1.839 Kg and as expected, in all cases the allele derived from sika conferred lower carcass mass. The sika population was fixed for all small carcass mass alleles, whereas the red deer population was typically polymorphic. GO term analysis of genes lying in the QTL regions are associated with oxygen transport. Although body mass is a likely target of selection, none of the SNPs marking QTL are introgressing faster or slower than expected in either direction.

evolutionary biology↗

bioRxiv2021

Genomic analysis reveals a polygenic architecture of antler morphology in wild red deer (Cervus elaphus).

Sexually-selected traits show large variation and rapid evolution across the animal kingdom, yet genetic variation often persists within populations despite apparent directional selection. A key step in solving this long-standing paradox is to determine the genetic architecture of sexually-selected traits to understand evolutionary drivers and constraints at the genomic level. Antlers are a form of sexual weaponry in male red deer. On the island of Rum, Scotland, males with larger antlers have increased breeding success, yet there has been no response to selection observed at the genetic level. To better understand the underlying mechanisms of this observation, we investigate the genetic architecture of ten antler traits and their principle components using genomic data from >38,000 SNPs. We estimate the heritabilities and genetic correlations of the antler traits using a genomic relatedness approach. We then use genome-wide association and haplotype-based regional heritability to identify regions of the genome underlying antler morphology, and an Empirical Bayes approach to estimate the underlying distributions of allele effect sizes. We show that antler morphology is heritable with a polygenic architecture, highly repeatable over an individuals lifetime, and that almost all aspects are positively genetically correlated with some loci identified as having pleiotropic effects. Our findings suggest that a large mutational target and pleiotropy with traits sharing similar complex polygenic architectures are likely to contribute to the maintenance of genetic variation in antler morphology in this population.

evolutionary biology↗

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↗

bioRxiv2021

Mutation load decreases with haplotype age in wild Soay sheep

Runs of homozygosity (ROH) are pervasive in diploid genomes and expose the effects of deleterious recessive mutations, but how exactly these regions contribute to variation in fitness remains unclear. Here, we combined empirical analyses and simulations to explore the deleterious effects of ROH with varying genetic map lengths in wild Soay sheep. Using a long-term dataset of 4,592 individuals genotyped at 417K SNPs, we found that inbreeding depression increases with ROH length. A 1% genomic increase in long ROH (>12.5cM) reduced the odds of first-year survival by 12%, compared to only 7% for medium ROH (1.56-12.5cM), while short ROH (<1.56cM) had no effect on survival. We show by forward genetic simulations that this is predicted: compared with shorter ROH, long ROH will have higher densities of deleterious alleles, with larger average effects on fitness and lower population frequencies. Taken together, our results are consistent with the idea that the mutation load decreases in older haplotypes underlying shorter ROH, where purifying selection has had more time to purge deleterious mutations. Finally, our study demonstrates that strong inbreeding depression can persist despite ongoing purging in a historically small population.

evolutionary biology↗

bioRxiv2021

Using genomic prediction to detect microevolutionary change of a quantitative trait

Detecting microevolutionary responses to natural selection by observing temporal changes in individual breeding values is challenging. The collection of suitable datasets can take many years and disentangling the contributions of the environment and genetics to phenotypic change is not trivial. Furthermore, pedigree-based methods of obtaining individual breeding values have known biases. Here, we apply a genomic prediction approach to estimate breeding values of adult weight in a 35-year dataset of Soay sheep (Ovis aries). During the study period adult body weight decreased, but the underlying genetic component of body weight increased, at a rate that is unlikely to be attributable to genetic drift. Thus cryptic microevolution of greater adult body weight has probably occurred. Using genomic prediction to study microevolution in wild populations can remove the requirement for pedigree data, potentially opening up new study systems for similar research.

evolutionary biology↗

bioRxiv2020

An investigation of MHC-dependent sexual selection in a free-living population of sheep

The MHC is one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. Apart from pathogen-mediated selection, sexual selection can also contribute to the maintenance of MHC diversity. MHC-dependent sexual selection could occur via several mechanisms but at present there is no consensus as to which of these mechanisms are involved and their importance. Previous studies have often suffered from limited genetic and behavioural data and small sample size, and were rarely able to examine all the mechanisms together, determine whether signatures of MHC-based non-random mating are independent of genomic effects or differentiate whether MHC-dependent sexual selection takes place at the pre- or post-copulatory stage. In this study, we use Monte Carlo simulation to investigate evidence for non-random MHC-dependent mating patterns by all three mechanisms in a free-living population of Soay sheep. Using 1710 sheep diplotyped at the MHC class IIa region and genome-wide SNPs, together with field observations of consorts, we found sexual selection against a particular haplotype in males at the pre-copulatory stage and sexual selection against female MHC heterozygosity during the rut. We also found MHC-dependent disassortative mating at the post-copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC-dependent disassortative mating could be a by-product of inbreeding avoidance. Our results therefore suggest that while multiple apparent mechanisms of non-random mating with respect to the MHC may occur, some of them have alternative explanations.

evolutionary biology↗

bioRxiv2020

Locus-specific introgression in young hybrid swarms: drift dominates selection

Closely related species that have previously inhabited geographically separated ranges are hybridizing at an increasing rate due to human disruptions. These anthropogenic hybrid zones can be used to study reproductive isolation between species at secondary contact, including examining locus-specific rates of introgression. Introgression is expected to be heterogenous across the genome, reflecting variation in selection. Those loci that introgress especially slowly are good candidates for being involved in reproductive isolation, while those loci that introgress quickly may be involved in adaptive introgression. In the context of conservation, policy makers are especially concerned about introduced alleles moving quickly into the background of a native or endemic species, as these alleles could replace the native alleles in the population, leading to extinction via hybridization. We applied genomic cline analyses to 44997 SNPs to identify loci introgressing at excessive rates when compared to the genome wide expectation in an anthropogenic hybridizing population of red deer and sika in Kintyre Scotland. We found 11.4% of SNPs had cline centers that were significantly different from the genome wide expectation, and 17.6% had excessive rates of introgression. Based on simulations, we believe that many of these markers have diverged from average due to drift, rather than because of selection. Future work could determine the policy implications of allelic-replacement due to drift rather than selection, and could use replicate, geographically distinct hybrid zones to narrow down those loci that are indeed responding to selection in anthropogenic hybrid zones.

evolutionary biology↗

bioRxiv2020

Selection of lamb size and early pregnancy in Soay sheep (Ovies aries)

The paradox of stasis - the unexpectedly slow evolution of heritable traits under direct selection - has been widely documented in the last few decades. This paradox is often particularly acute for body size, which is often heritable and where positive associations of size and fitness are frequently identified, but constraints to the evolution of larger body sizes are often not obvious. Here, we identify a trade-off between survival and size-dependent reproduction in Soay sheep (Ovis aries), contributes to selection against large body size. Using recently developed theory on non-linear developmental systems, then decompose total selection of ewe lamb mass along different causal paths to fitness. Larger lambs are more likely to become pregnant, which has a large viability cost. After controlling for this pathway, however, the association between lamb mass and subsequent lifetime fitness is positive. Thus this trade-off does not fully explain stasis of size in tis population, but it does substantially reduce the strength of positive directional selection of size that would otherwise occur. While selection currently favours reduced probability of early pregnancy, largely irrespective of body size, it is likely that the occurrence of early pregnancy could result from adaptation to conditions during a recent period during which population density was much lower.

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

Variants at RNF212 and RNF212B are associated with recombination rate variation in Soay sheep (Ovis aries).

Meiotic recombination is a ubiquitous feature of sexual reproduction, ensuring proper disjunction of homologous chromosomes, and creating new combinations of alleles upon which selection can act. By identifying the genetic drivers of recombination rate variation, we can begin to understand its evolution. Here, we revisit an analysis investigating the genetic architecture of gamete autosomal crossover counts (ACC) in a wild population of Soay sheep (Ovis aries) using a much larger dataset (increasing from 3,300 to 7,235 gametes and from [~]39,000 to [~]415,000 SNPs for genome-wide association analysis). Animal models fitting genomic relatedness confirmed that ACC was heritable in both females (h2 = 0.18) and males (h2 = 0.12). Genome-wide association studies identified two regions associated with ACC variation. A region on chromosome 6 containing RNF212 explained 46% of heritable variation in female ACC, but was not associated with male ACC, confirming the previous finding. A region on chromosome 7 containing RNF212B explained 20-25% of variation in ACC in both males and females. Both RNF212 and RNF212B have been repeatedly associated with recombination rate in other mammal species. These findings confirm that moderate to large effect loci can underpin ACC variation in wild mammals, and provide a foundation for further studies on the evolution of recombination rates.

genetics↗

bioRxiv2020

Haplotyping MHC class IIa by high throughput screening in an isolated sheep population

Investigating the current evolutionary processes acting on a highly polymorphic gene region, such as the major histocompatibility complex (MHC), requires extensive population data for both genotypes and phenotypes. The MHC consists of several tightly linked loci with both allelic and gene content variation, making it challenging to genotype. Eight class IIa haplotypes have previously been identified in the Soay sheep (Ovis aries) of St. Kilda using Sanger sequencing and cloning, but no single locus is representative of all haplotypes. Here, we exploit the closed nature of the island population of Soay sheep and its limited haplotypic variation to identify a panel of SNPs that enable imputation of MHC haplotypes. We compared MHC class IIa haplotypes determined by Sanger sequence-based genotyping of 135 individuals to their SNP profiles generated using the Ovine Infinium HD BeadChip. A panel of 11 SNPs could reliably determine MHC diplotypes, and two additional SNPs within the DQA1 gene enabled detection of a recombinant haplotype affecting only the SNPs downstream of the expressed genes. The panel of 13 SNPs was genotyped in 5951 Soay sheep, of which 5349 passed quality control. Using the Soay sheep pedigree, we were able to trace the origin and inheritance of the recombinant SNP haplotype. This SNP-based method has enabled the rapid generation of locus-specific MHC genotypes for large numbers of Soay sheep. This volume of high-quality genotypes in a well-characterized population of free-living sheep will be valuable for investigating the mechanisms maintaining diversity at the MHC.

evolutionary biology↗

bioRxiv2020

Genomic prediction in the wild: A case study in Soay sheep

Genomic prediction, the technique whereby an individuals genetic component of their phenotype is estimated from its genome, has revolutionised animal and plant breeding and medical genetics. However, despite being first introduced nearly two decades ago, it has hardly been adopted by the evolutionary genetics community studying wild organisms. Here, genomic prediction is performed on eight traits in a wild population of Soay sheep. The population has been the focus of a >30 year evolutionary ecology study and there is already considerable understanding of the genetic architecture of the focal Mendelian and quantitative traits. We show that the accuracy of genomic prediction is high for all traits, but especially those with loci of large effect segregating. Five different methods are compared, and the two methods that can accommodate zero-effect and large-effect loci in the same model tend to perform best. If the accuracy of genomic prediction is similar in other wild populations, then there is a real opportunity for pedigree-free molecular quantitative genetics research to be enabled in many more wild populations; currently the literature is dominated by studies that have required decades of field data collection to generate sufficiently deep pedigrees. Finally, some of the potential applications of genomic prediction in wild populations are discussed.

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↗

bioRxiv2020

Genetic architecture and lifetime dynamics of inbreeding depression in a wild mammal

Inbreeding depression is ubiquitous, but we still know little about its genetic architecture and precise effects in wild populations. Here, we combine long-term life-history data with 417K imputed SNP genotypes for 5,952 wild Soay sheep to explore inbreeding depression on a key fitness component, annual survival. Inbreeding manifests in long runs of homozygosity (ROH), which make up nearly half of the genome in the most inbred individuals. The ROH landscape varies widely across the genome, with islands where up to 87% and deserts where only 4% of individuals have ROH. The fitness consequences of inbreeding are severe; a 10% increase in individual inbreeding FROH is associated with a 60% reduction in the odds of survival in lambs, though inbreeding depression decreases with age. Finally, a genome-wide association scan on ROH shows that many loci with small effects and five loci with larger effects contribute to inbreeding depression in survival.

evolutionary biology↗

bioRxiv2020

A rare MHC haplotype confers selective advantage in a free-living ruminant

Genes within the major histocompatibility complex (MHC) are the most variable identified in vertebrates. Pathogen-mediated selection (PMS) is believed to be the main force maintaining diversity at MHC class I and II genes, but it has proven hard to demonstrate the exact PMS regime that is acting in natural populations. Demonstrating contemporary selection on MHC alleles is not trivial, and previous work has been constrained by limited genetic tools, low sample sizes and short time scales and has sometimes involved anticonservative statistical approaches. Here, we use appropriate statistical approaches to examine associations between MHC variation and several fitness measurements including total fitness (lifetime breeding success) and five fitness components, in 3400 wild Soay sheep (Ovis aries) monitored over their lifetimes between 1989 and 2012. We found haplotypes C and D were associated with decreased and increased male total fitness respectively. In terms of fitness components, juvenile survival was positively associated with haplotype divergence. Of the eight MHC haplotypes (A-H), haplotypes C and F were associated with decreased adult male breeding success and decreased adult female life span respectively. Consistent with the increased male total fitness, haplotype D, which is the rarest, has increased in frequency throughout the study period. Our results suggest that contemporary balancing selection is acting on MHC class II genes in Soay sheep and that different selection mechanisms are acting between juveniles and adults.

evolutionary biology↗