Individuals and populations

Clutton‐Brock, T. H.; Pemberton, J. M.

doi:10.1017/cbo9780511550669.001

Cited by 61 publications

(118 citation statements)

References 532 publications

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“…comm.). However since this is an isolated population, subject to regular population crashes [14], the absence of polymorphism in BMP15 in this population may not be overly surprising and further studies in other wild sheep populations are warranted.…”

Section: Resultsmentioning

confidence: 88%

Heterozygote Advantage for Fecundity

Gemmell

Slate

2006

PLoS ONE

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Heterozygote advantage, or overdominance, remains a popular and persuasive explanation for the maintenance of genetic variation in natural populations in the face of selection. However, despite being first proposed more than 80 years ago, there remain few examples that fit the criteria for heterozygote advantage, all of which are associated with disease resistance and are maintained only in the presence of disease or other gene-by-environment interaction. Here we report five new examples of heterozygote advantage, based around polymorphisms in the BMP15 and GDF9 genes that affect female fecundity in domesticated sheep and are not reliant on disease for their maintenance. Five separate mutations in these members of the transforming growth factor β (TGFβ) superfamily give phenotypes with fitness differentials characteristic of heterozygous advantage. In each case, one copy of the mutant allele increases ovulation rate, and ultimately litter size per ewe lambing, relative to the wildtype. However, homozygous ewes inheriting mutant alleles from both parents have impaired oocyte development and maturation, which results in small undeveloped ovaries and infertility. Using data collected over many years on ovulation rates, litter size, and lambing rates, we have calculated the equilibrium solution for each of these polymorphisms using standard population genetic theory. The predicted equilibrium frequencies obtained for these mutant alleles range from 0.11 to 0.23, which are amongst the highest yet reported for a polymorphism maintained by heterozygote advantage. These are amongst the most frequent and compelling examples of heterozygote advantage yet described and the first documented examples of heterozygote advantage that are not reliant on a disease interaction for their maintenance.

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Section: Resultsmentioning

confidence: 88%

Heterozygote Advantage for Fecundity

Gemmell

Slate

2006

PLoS ONE

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“…The development of immunity to gastrointestinal nematodes (GIN) parasites including Tc is thought to be antibody‐mediated in sheep (Stear, Park, & Bishop, 1996), and experimental studies show that antibody responses increase with age as the immune response develops (Nguyen, 1984; Smith, Jackson, Jackson, & Williams, 1985; Watson, Colditz, Andrew, Gill, & Altmann, 1994). All individuals are exposed to these parasites from very early life on St Kilda (Wilson, Grenfell, Pilkington, Boyd, & Gulland, 2004), so it is likely that the population‐level increase in antibody levels reflects the steady development of the immune response to these worms over the animals’ first few years. Clear and progressive declines in the proportions of naïve T cells have previously been reported in this population from a smaller sample of animals (Nussey et al., 2012).…”

Section: Discussionmentioning

confidence: 99%

Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival

Watson

McNeilly

Watt

et al. 2016

Ecology and Evolution

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Immune defenses are expected to be crucial for survival under the considerable parasite pressures experienced by wild animals. However, our understanding of the association between immunity and fitness in nature remains limited due to both the complexity of the vertebrate immune system and the often‐limited availability of immune reagents in nonmodel organisms. Here, we use methods and reagents developed by veterinary researchers for domestic ungulates on blood samples collected from a wild Soay sheep population, to evaluate an unusually broad panel of immune parameters. Our evaluation included different innate and acquired immune cell types as well as nematode parasite‐specific antibodies of different isotypes. We test how these markers correlate with one another, how they vary with age‐group and sex, and, crucially, whether they predict overwinter survival either within or among demographic groups. We found anticipated patterns of variation in markers with age, associated with immune development, and once these age trends were accounted for, correlations among our 11 immune markers were generally weak. We found that females had higher proportions of naïve T cells and gamma–delta T cells than males, independent of age, while our other markers did not differ between sexes. Only one of our 11 markers predicted overwinter survival: sheep with higher plasma levels of anti‐nematode IgG antibodies were significantly more likely to survive the subsequent high mortality winter, independent of age, sex, or weight. This supports a previous finding from this study system using a different set of samples and shows that circulating antibody levels against ecologically relevant parasites in natural systems represent an important parameter of immune function and may be under strong natural selection. Our data provide rare insights into patterns of variation among age‐ and sex groups in different T‐cell subsets and antibody levels in the wild, and suggest that certain types of immune response—notably those likely to be repeatable within individuals and linked to resistance to ecologically relevant parasites—may be most informative for research into the links between immunity and fitness under natural conditions.

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“…Since 1985, the individuals resident in the Village Bay area of Hirta have been the subject of long-term individual-based monitoring [34]. Individuals are caught and marked at birth in spring, and each August we re-capture as many sheep from the study population as possible using temporary traps.…”

Section: Methodsmentioning

confidence: 99%

“…1500 g ) for 10 min, and the plasma is removed and stored at −20°C. Nematode eggs in faecal samples are counted shortly after collection, and strongyle FEC is estimated as the number of eggs per gram using a modified McMaster technique (following [21]; see [34] for further details of the population's history and fieldwork). On St Kilda, five nematode species contribute to this count, the most abundant being T. circumcincta , Trichostrongylus axei and Trichostrongylus vitrinus [35].…”

Section: Methodsmentioning

confidence: 99%

Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival

et al. 2014

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Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circulating in vivo reflect a composite of constitutive and induced functional variants of diverse specificities (e.g. binding antigens from prevalent parasites, self tissues or novel non-self sources). Here, we measured plasma concentrations of 11 different antibody types in adult females from an unmanaged population of Soay sheep on St Kilda. Correlations among antibody measures were generally positive but weak, and eight of the measures independently predicted body mass, strongyle parasite egg count or survival over the subsequent winter. These independent and, in some cases, antagonistic relationships point to important multivariate immunological heterogeneities affecting organismal health and fitness in natural systems. Notably, we identified a strong positive association between anti-nematode immunoglobulin (Ig) G antibodies in summer and subsequent over-winter survival, providing rare evidence for a fitness benefit of helminth-specific immunity under natural conditions. Our results highlight both the evolutionary and ecological importance and the complex nature of the immune phenotype in the wild.

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Individuals and populations

Cited by 61 publications

References 532 publications

Heterozygote Advantage for Fecundity

Heterozygote Advantage for Fecundity

Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival

Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival

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