Biology subjects

Pemberton, J. M.

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

44 records · Page 3Linked to original sources

bioRxiv2019

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

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

ecology↗

bioRxiv2019

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

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

genetics↗

bioRxiv2019

Increased genetic marker density reveals high levels of admixture between red deer and introduced sika in Kintyre, Scotland

Hybridization is a natural process at species range boundaries, but increasing numbers of species are hybridizing due to direct or indirect human activities. In such cases of anthropogenic hybridization, subsequent introgression can threaten the survival of native species. To date many such systems have been studied with too few genetic markers to assess the level of threat resulting from advanced backcrossing. Here we use 44,999 single nucleotide polymorphisms and the ADMIXTURE program to study two areas of Scotland where a panel of 22 diagnostic microsatellites previously identified introgression between native red deer (Cervus elaphus) and introduced Japanese sika (Cervus nippon). In Kintyre we reclassify 26% of deer from the pure species categories to the hybrid category whereas in the NW Highlands we only reclassify 2%. As expected, the reclassified individuals are mostly advanced backcrosses. We also investigate the ability of marker panels selected on different posterior allele frequency criteria to find hybrids assigned by the full marker set, and show that in our data, ancestry informative markers (i.e. those that are highly differentiated between the species, but not fixed) are better than diagnostic markers (those markers that are fixed between the species) because they are more evenly distributed in the genome. Diagnostic loci are concentrated on the X chromosome to the detriment of autosomal coverage.

evolutionary biology↗

bioRxiv2018

RAD-sequencing for estimating GRM-based heritability in the wild: a case study in roe deer

Estimating the evolutionary potential of quantitative traits and reliably predicting responses to selection in wild populations are important challenges in evolutionary biology. The genomic revolution has opened up opportunities for measuring relatedness among individuals with precision, enabling pedigree-free estimation of trait heritabilities in wild populations. However, until now, most quantitative genetic studies based on a genomic relatedness matrix (GRM) have focused on long-term monitored populations for which traditional pedigrees were also available, and have often had access to knowledge of genome sequence and variability. Here, we investigated the potential of RAD-sequencing for estimating heritability in a free-ranging roe deer population for which no prior genomic resources were available. We propose a step-by-step analytical framework to optimize the quality and quantity of the genomic data and explore the impact of the SNP calling and filtering processes on the GRM structure and GRM-based heritability estimates. As expected, our results show that sequence coverage strongly affects the number of recovered loci, the genotyping error rate and the amount of missing data. Ultimately, this had little effect on heritability estimates and their standard errors, provided that the GRM was built from a minimum number of loci (above 7000). GRM-based heritability estimates thus appear robust to a moderate level of genotyping errors in the SNP dataset. We also showed that quality filters, such as the removal of low-frequency variants, affect the relatedness structure of the GRM, generating lower h2 estimates. Our work illustrates the huge potential of RAD-sequencing for estimating GRM-based heritability in virtually any natural population.

genomics↗

bioRxiv2018

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

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

ecology↗

bioRxiv2018

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

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

ecology↗

bioRxiv2018

A genomic region containing REC8 and RNF212B is associated with individual recombination rate variation in a wild population of red deer (Cervus elaphus)

Recombination is a fundamental feature of sexual reproduction, ensuring proper disjunction, preventing mutation accumulation and generating new allelic combinations upon which selection can act. However it is also mutagenic, and breaks up favourable allelic combinations previously built up by selection. Identifying the genetic drivers of recombination rate variation is a key step in understanding the causes and consequences of this variation, how lociassociated with recombination are evolving and how they affect the potential of a population to respond to selection. However, to date, few studies have examined the genetic architecture of recombination rate variation in natural populations. Here, we use pedigree data from -2,600 individuals genotyped at -38,000 SNPs to investigate the genetic architecture of individual autosomal recombination rate in a wild population of red deer (Cervus elaphus). Female red deer exhibited a higher mean and phenotypic variance in autosomal crossover counts (ACC). Animal models fitting genomic relatedness matrices showed that ACC was heritable in females (h2 = 0.12) but not in males. A regional heritability mapping approach showed that almost all heritable variation in female ACC was explained by a genomic region on deer linkage group 12 containing the candidate loci REC8 and RNF212B, with an additional region on linkage group 32 containing TOP2B approaching genome-wide significance. The REC8/RNF212B region and its paralogue RNF212 have been associated with recombination in cattle, mice, humans and sheep. Our findings suggest that mammalian recombination rates have a relatively conserved genetic architecture in both domesticated and wild systems, and provide a foundation for understanding the association between recombination lociand individual fitness within this population.

genetics↗

bioRxiv2017

A high-density linkage map reveals sexually-dimorphic recombination landscapes in red deer (Cervus elaphus)

High density linkage maps are an important tool to gain insight into the genetic architecture of traits of evolutionary and economic interest, and provide a resource to characterise variation in recombination landscapes. Here, we used information from the cattle genome and the 50K Cervine Illumina BeadChip to inform and refine a high density linkage map in a wild population of red deer (Cervus elaphus). We constructed a predicted linkage map of 38,038 SNPs and a skeleton map of 10,835 SNPs across 34 linkage groups. We identified several chromosomal rearrangements in the deer lineage relative to sheep and cattle, including six chromosome fissions, one fusion and two large inversions. Otherwise, our findings showed strong concordance with map orders in the cattle genome. The sex-averaged linkage map length was 2739.7cM and the genome-wide autosomal recombination rate was 1.04cM per Mb. The female autosomal map length was 1.21 longer than that of males (2767.4cM vs 2280.8cM, respectively). Sex differences in map length were driven by high female recombination rates in peri-centromeric regions, a pattern that is unusual relative to other mammal species. This effect was more pronounced in fission chromosomes that would have had to produce new centromeres. We propose two hypotheses to explain this effect: (1) that this mechanism may have evolved to counteract centromeric drive associated with meiotic asymmetry in oocyte production; and/or (2) that sequence and structural characteristics suppressing recombination in close proximity to the centromere may not have yet evolved at neo-centromeres. Our study provides insight into how recombination landscapes vary and evolve in mammals, and will provide a valuable resource for studies of evolution, genetic improvement and population management in red deer and related species.\n\nArticle SummaryWe present a high density linkage map (>38,000 markers) in a wild population of Red deer (Cervus elaphus). Our investigation of the recombination landscape showed a marked difference in recombination rates between the sexes in proximity to the centromere, with females showing an unusually elevated rate relative to other mammal species. This effect is most pronounced in chromosomes that would have produced a new centromere in the deer lineage. We propose that the observed effects have evolved to counteract selfish genetic elements associated with asymmetrical female meiosis.

genomics↗