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Heterozygosity-fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (Capra ibex).

ABSTRACT: Crucial for the long-term survival of wild populations is their ability to fight diseases. Disease outbreaks can lead to severe population size reductions, which makes endangered and reintroduced species especially vulnerable. In vertebrates, the major histocompatibility complex (MHC) plays an important role in determining the immune response. Species that went through severe bottlenecks often show very low levels of genetic diversity at the MHC. Due to the known link between the MHC and immune response, such species are expected to be at particular risk in case of disease outbreaks. However, so far, only few studies have shown that low MHC diversity is correlated with increased disease susceptibility in species after severe bottlenecks. We investigated genetic variation at the MHC and its correlations with disease resistance and other fitness-related traits in Alpine ibex (Capra ibex), a wild goat species that underwent a strong bottleneck in the last century and that is known to have extremely low genetic variability, both genome-wide and at the MHC. We studied MHC variation in male ibex of Gran Paradiso National Park, the population used as a source for all postbottleneck reintroductions. We found that individual MHC heterozygosity (based on six microsatellites) was not correlated with genome-wide neutral heterozygosity. MHC heterozygosity, but not genome-wide heterozygosity, was positively correlated with resistance to infectious keratoconjunctivitis and with body mass. Our results show that genetic variation at the MHC plays an important role in disease resistance and, hence, should be taken into account for successfully managing species conservation.

SUBMITTER: Brambilla A

PROVIDER: S-EPMC5979623 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Heterozygosity-fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (<i>Capra ibex</i>).

Brambilla Alice A Keller Lukas L Bassano Bruno B Grossen Christine C

Evolutionary applications 20171204 5

Crucial for the long-term survival of wild populations is their ability to fight diseases. Disease outbreaks can lead to severe population size reductions, which makes endangered and reintroduced species especially vulnerable. In vertebrates, the major histocompatibility complex (MHC) plays an important role in determining the immune response. Species that went through severe bottlenecks often show very low levels of genetic diversity at the MHC. Due to the known link between the MHC and immune ...[more]

PMID: 29875807

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Project description:The major histocompatibility complex (MHC) is a crucial component of the vertebrate immune system and shows extremely high levels of genetic polymorphism. The extraordinary genetic variation is thought to be ancient polymorphisms maintained by balancing selection. However, introgression from related species was recently proposed as an additional mechanism. Here we provide evidence for introgression at the MHC in Alpine ibex (Capra ibex ibex). At a usually very polymorphic MHC exon involved in pathogen recognition (DRB exon 2), Alpine ibex carried only two alleles. We found that one of these DRB alleles is identical to a DRB allele of domestic goats (Capra aegagrus hircus). We sequenced 2489 bp of the coding and non-coding regions of the DRB gene and found that Alpine ibex homozygous for the goat-type DRB exon 2 allele showed nearly identical sequences (99.8%) to a breed of domestic goats. Using Sanger and RAD sequencing, microsatellite and SNP chip data, we show that the chromosomal region containing the goat-type DRB allele has a signature of recent introgression in Alpine ibex. A region of approximately 750 kb including the DRB locus showed high rates of heterozygosity in individuals carrying one copy of the goat-type DRB allele. These individuals shared SNP alleles both with domestic goats and other Alpine ibex. In a survey of four Alpine ibex populations, we found that the region surrounding the DRB allele shows strong linkage disequilibria, strong sequence clustering and low diversity among haplotypes carrying the goat-type allele. Introgression at the MHC is likely adaptive and introgression critically increased MHC DRB diversity in the genetically impoverished Alpine ibex. Our finding contradicts the long-standing view that genetic variability at the MHC is solely a consequence of ancient trans-species polymorphism. Introgression is likely an underappreciated source of genetic diversity at the MHC and other loci under balancing selection.

Project description:BACKGROUND:Defining hidden genetic diversity within species is of great significance when attempting to maintain the evolutionary potential of natural populations and conduct appropriate management. Our hypothesis is that isolated (and eventually small) wild animal populations hide unexpected genetic diversity due to their maintenance of ancient polymorphisms or introgressions. RESULTS:We tested this hypothesis using the Iberian ibex (Capra pyrenaica) as an example. Previous studies based on large sample sizes taken from its principal populations have revealed that the Iberian ibex has a remarkably small MHC DRB1 diversity (only six remnant alleles) as a result of recent population bottlenecks and a marked demographic decline that has led to the extinction of two recognized subspecies. Extending on the geographic range to include non-studied isolated Iberian ibex populations, we sequenced a new MHC DRB1 in what seemed three small isolated populations in Southern Spain (n?=?132). The findings indicate a higher genetic diversity than previously reported in this important gene. The newly discovered allele, MHC DRB1*7, is identical to one reported in the domestic goat C. aegagrus hircus. Whether or not this is the result of ancient polymorphisms maintained by balancing selection or, alternatively, introgressions from domestic goats through hybridization needs to be clarified in future studies. However, hybridization between Iberian ibex and domestic goats has been reported in Spain and the fact that the newly discovered allele is only present in one of the small isolated populations and not in the others suggests introgression. The new discovered allele is not expected to increase fitness in C. pyrenaica since it generates the same protein as the existing MHC DRB1*6. Analysis of a microsatellite locus (OLADRB1) near the new MHC DRB1*7 gene reveals a linkage disequilibrium between these two loci. The allele OLADRB1, 187 bp in length, was unambiguously linked to the MHC DRB1*7 allele. This enabled us to perform a DRB-STR matching method for the recently discovered MHC allele. CONCLUSIONS:This finding is critical for the conservation of the Iberian ibex since it directly affects the identification of the units of this species that should be managed and conserved separately (Evolutionarily Significant Units).

Project description:BackgroundSarcoptic mange is one of the main parasitic diseases affecting the Iberian ibex Capra pyrenaica. Scabietic animals suffer a decline in body condition and reproductive fitness and in severe cases may die. Although several previous studies of the pathology of this disease and the physiological changes it produces in ibex have been carried out in recent years, our knowledge of the relationship between Sarcoptes scabiei and other ectoparasites of this host is still limited.MethodsWe analysed 430 Iberian ibex skin samples. Ectoparasites were removed, counted and identified. Mite (S. scabiei) numbers were obtained after digesting the skin samples in a 5% KOH solution. We modelled mite numbers in terms of host sex and age, site, year, season and the presence of other ectoparasites such as ticks and lice using generalized linear mixed models (GLMMs) and ectoparasite co-occurrence patterns using two different models: the probabilistic model species co-occurrence and the generalized linear latent variable model (GLLVM).ResultsThe ectoparasite community was mainly composed of S. scabiei, six ticks (Haemaphysalis sulcata, Haemaphysalis punctata, Rhipicephalus bursa, Rhipicephalus turanicus, Dermacentor marginatus and Ixodes ricinus) and two lice (Bovicola crassipes and Linognathus stenopsis). Adult male ibex harboured more mites than females. Mite numbers varied greatly spatially and seasonally and increased with the presence of other parasites. Some positive co-occurrence relationships between pairs of different ectoparasites were observed, particularly between ticks. The presence of S. scabiei negatively affected lice and H. sulcata numbers.ConclusionsSarcoptic mange has spread above all in ibex populations in and around the Mediterranean Basin, where it is now found in almost a third of its host's range. Mite numbers varied seasonally and spatially and were higher in male hosts. The presence of S. scabiei had a negative effect on lice numbers but favoured the presence of ticks.

Dataset Information

Heterozygosity-fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (Capra ibex).

Publications

Heterozygosity-fitness correlation at the major histocompatibility complex despite low variation in Alpine ibex (<i>Capra ibex</i>).

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