Biology subjects

Johnston, S. E.

Publications and source records attributed to Johnston, S. E..

At least 19 recordsLinked to original sources

bioRxiv2024

Individual variation in meiotic crossover positioning, rate and interference are driven by distinct genetic processes in domestic pigs.

Meiotic crossovers are essential for proper chromosome segregation, and provide an important mechanism for adaptation through linking beneficial alleles and purging deleterious mutations. However, crossovers can also break apart beneficial alleles and are themselves a source of new mutations within the genome. The rate and distribution of crossovers shows huge variation both within and between chromosomes, individuals and species, yet the molecular and evolutionary causes and consequences of this variation remain poorly understood. A key step in understanding this variation is to understand the genetic architecture of how many crossovers occur, where they occur, and how they interfere, as this allows us to identify the degree to which these factors are governed by common or distinct genetic processes. Here, we investigate individual variation in crossover count, crossover interference ({nu}), and crossover positioning measured as both intra-chromosomal allelic shuffling and distance to telomere (Mb), in a large genotyped breeding population of domestic pigs. Using measures from 82,474 gametes from 4,704 mothers and 271 fathers, we show that crossover traits are heritable within each sex (h2 = 0.03 - 0.11), with the exception of male crossover interference. Crossover count and interference have a strongly shared genetic architecture in females, mostly driven by variants at RNF212. Female crossover positioning is mediated by variants at MEI4, PRDM9, and SYCP2. We also identify tentative associations at genomic regions corresponding to CTCF and REC114/REC8/CCNB1IP1 (crossover count), and ZCWPW1 and ZCWPW2 (crossover positioning). Our results show that crossover count and crossover positioning in female pigs have the capacity to evolve somewhat independently in our dataset.

genomics↗

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

Genetic architecture of individual meiotic crossover rate and distribution in a large Atlantic Salmon (Salmo salar) breeding population.

Meiotic recombination through chromosomal crossovers ensures proper segregation of homologous chromosomes in meiosis, while also breaking down linkage disequilibrium and shuffling alleles at loci located on the same chromosome. Rates of recombination can vary between species, but also between and within individuals, sex and chromosomes within species. Indeed, the Atlantic salmon genome is known to have clear sex differences in recombination with female biased heterochiasmy and markedly different landscapes of crossovers between males and females. In male meiosis, crossovers occur strictly in the telomeric regions, whereas in female meiosis crossovers tend to occur closer to the centromeres. However, little is known about the genetic control of these patterns and how this differs at the individual level. Here, we investigate genetic variation in individual measures of recombination in >5000 large full-sib families of a Norwegian Atlantic salmon breeding population with high-density SNP genotypes. We show that females had 1.6x higher crossover counts (CC) than males, with autosomal linkage maps spanning a total of 2174 cM in females and 1483 cM in males. However, because of the extreme telomeric bias of male crossovers, female recombination is much more important for generation of new haplotypes with 8x higher intra-chromosomal genetic shuffling than males. CC was heritable in females (h2 = 0.11) and males (h2 = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h2 = 0.06) than in males (h2 = 0.11). Inter-sex genetic correlations for both traits were close to zero, suggesting that rates and distribution of crossovers are genetically distinct traits in males and females, and that there is a potential for independent genetic change in both sexes in the Atlantic Salmon. Together, these findings give novel insights into the genetic architecture of recombination in salmonids and contribute to a better understanding of how rates and distribution of recombination may evolve in eukaryotes more broadly.

genetics↗

bioRxiv2023

Sex-differences in the genetic architecture of individual recombination rates in wild house sparrows (Passer domesticus).

Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver of genomic diversity. It ensures proper disjunction, allows increased selection responses, and prevents mutation accumulation; however, it is also mutagenic and can break up favourable haplotypes. This cost/benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation in nature. Identifying the genetic architecture of this variation is key to understanding its causes and consequences. Here, we investigate individual recombination rate variation in wild house sparrows (Passer domesticus). We integrate genomic and pedigree data to identify autosomal crossover counts (ACC) and intra-chromosomal allelic shuffling ([r]intra) in 13,056 gametes. Females had 1.37 times higher ACC, and 1.55 times higher[r] intra than males. ACC and[r] intra were heritable in females and males (ACC h2 = 0.23 and 0.11;[r] intra h2 = 0.12 and 0.14), but cross-sex additive genetic correlations were low (rA = 0.29 and 0.32 for ACC and[r] intra). Conditional bivariate analyses showed that all measures remained heritable after accounting for genetic values in the opposite sex, indicating that sex-specific ACC and[r] intra can evolve somewhat independently. Genome-wide models showed that ACC and[r] intra are polygenic and driven by many small-effect loci, many of which are likely to act in trans as global recombination modifiers. Our findings show that recombination rates of females and males can have different evolutionary potential in wild birds, providing a compelling mechanism for the evolution of sexual dimorphism in recombination.

genetics↗

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

Variation in mutation, recombination, and transposition rates in Drosophila melanogaster and Drosophila simulans

Mutation, recombination, and transposition occurring during meiosis provide the variation on which natural selection can act and the rates at which they occur are important parameters in models of evolution. The de novo mutation rate determines levels of genetic diversity, responses to ongoing selection, and levels of genetic load. Recombination breaks up haplotypes and reduces the effects of linkage, helping to spread beneficial alleles and purge deleterious ones. Transposable elements (TE) selfishly replicate themselves through the genome, imposing fitness costs on the host and introducing complex mutations that can affect gene expression and give rise to new genes. However, even for key evolutionary models such as Drosophila melanogaster and D. simulans few estimates of these parameters are available, and we have little idea of how rates vary between individuals, sexes, populations, or species. Here, we provide direct estimates of mutation, recombination, and transposition rates and their variation in a West African and a European population of D. melanogaster and a European population of D. simulans. Across 89 flies, we observe 58 single nucleotide mutations, 286 crossovers, and 89 TE insertions. Compared to the European D. melanogaster, we find the West African population has a lower mutation rate (1.67 vs. 4.86 x 10-9 site-1 gen-1) and transposition rate (8.99 vs. 23.36 x 10-5 copy-1 gen-1), but a higher recombination rate (3.44 vs. 2.06 cM/Mb). The European D. simulans population has a similar mutation rate to European D. melanogaster but a significantly higher recombination rate and a lower but not significantly different transposition rate. Overall, we find paternal-derived mutations are more frequent than maternal ones in both species. HighlightsO_LIDe novo mutation rates are 1.67 x 10-9 site-1 gen-1 (95% HPD CI: 0.54 - 3.14 x 10-9), 4.86 x 10-9 site-1 gen-1 (2.11 - 8.02 x 10-9), and 4.51 x 10-9 site-1 gen-1 (1.94 - 7.75 x 10-9) for the West African D. melanogaster, the European D. melanogaster and the European D. simulans population, respectively. C_LIO_LIIn females, recombination rates in the absence of large genomic inversions are 3.44 cM/Mb (2.72 - 4.18), 2.06 cM/Mb (1.57 - 2.57), and 3.04 cM/Mb (2.45 - 3.73) for the three populations, respectively. There was no strong evidence of recombination observed in males. C_LIO_LIMutations (SNMs and indels) are male-biased. C_LIO_LIThe West African D. melanogaster population has a lower TE activity than the other populations and CMC-Transib is the dominant active TE. The European D. melanogaster population has multiple active TEs: Gypsy, CMC-Transib, Pao, Jockey and hAT-hobo; while in European D. simulans, they are Gypsy, CMC-Transib, Pao, hAT-hobo, Copia and TcMar-Mariner. C_LI

evolutionary biology↗

bioRxiv2021

Associations between MHC class II variation and phenotypic traits in a free-living sheep population

Pathogen-mediated selection (PMS) is thought to maintain the high level of allelic diversity observed in the major histocompatibility complex (MHC) class II genes. A comprehensive way to demonstrate contemporary selection is to examine associations between MHC variation and individual fitness. As individual fitness is hard to measure, many studies examine associations between MHC diversity and phenotypic traits which include direct or indirect measures of adaptive immunity thought to contribute to fitness. Here, we tested associations between MHC class II variation and five representative phenotypic traits measured in August: weight, strongyle faecal egg count, and plasma IgA, IgE and IgG immunoglobulin titres against the gastrointestinal nematode parasite Teladorsagia circumcincta in a free-living population of Soay sheep. We found no association between MHC class II variation and August weight or strongyle faecal egg count. We did however find associations between MHC class II variation and immunoglobulin levels which varied with age, isotype and sex. Our results suggest associations between MHC and phenotypic traits are more likely to be found for traits more closely associated with pathogen defence than integrative traits such as body weight and highlight a useful role of MHC-antibody associations in examining selection on MHC genes.

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

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

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

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↗

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↗