Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population

Niskanen, Alina K.; Kennedy, L. J.; Ruokonen, Minna; Kojola, Ilpo; Lohi, Hannes; Isomursu, Marja; Jansson, Eva; Pyhäjärvi, Tanja; Aspi, Jouni

doi:10.1111/mec.12647

Cited by 55 publications

(81 citation statements)

References 85 publications

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“…Niskanen et al . ) by types of balancing selection such as heterozygote advantage, frequency‐dependent selection and variable selection in time and space (Hedrick ).…”

Section: Introductionmentioning

confidence: 99%

Population genetic inferences using immune gene SNPs mirror patterns inferred by microsatellites

Elbers

Clostio

Taylor

2016

Molecular Ecology Resources

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Single nucleotide polymorphisms (SNPs) are replacing microsatellites for population genetic analyses, but it is not apparent how many SNPs are needed or how well SNPs correlate with microsatellites. We used data from the gopher tortoise, Gopherus polyphemus – a species with small populations, to compare SNPs and microsatellites to estimate population genetic parameters. Specifically, we compared one SNP dataset (16 tortoises from 4 populations sequenced at 17,901 SNPs) to two microsatellite datasets, a full dataset of 101 tortoises and a partial dataset of 16 tortoises previously genotyped at 10 microsatellites. For the full microsatellite dataset, observed heterozygosity, expected heterozygosity, and FST were correlated between SNPs and microsatellites; however, allelic richness was not. The same was true for the partial microsatellite dataset, except that allelic richness, but not observed heterozygosity, was correlated. The number of clusters estimated by Structure differed for each dataset (SNPs = 2; partial microsatellite = 3; full microsatellite = 4). PCA showed four clusters for all datasets. More than 800 SNPs were needed to correlate with allelic richness, observed heterozygosity, and expected heterozygosity, but only 100 were needed for FST. The number of SNPs typically obtained from NGS far exceeds the number needed to correlate with microsatellite parameter estimates. Our study illustrates that diversity, FST, and PCA results from microsatellites can mirror those obtained with SNPs. These results may be generally applicable to small populations, a defining feature of endangered and threatened species, because theory predicts that genetic drift will tend to outweigh selection in small populations.

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“…Niskanen et al . ) by types of balancing selection such as heterozygote advantage, frequency‐dependent selection and variable selection in time and space (Hedrick ).…”

Section: Introductionmentioning

confidence: 99%

Population genetic inferences using immune gene SNPs mirror patterns inferred by microsatellites

Elbers

Clostio

Taylor

2016

Molecular Ecology Resources

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“…In grey wolves, variation in MHC genes in individuals from Croatia and Finland was compatible with balancing selection (Niskanen et al. ), while in the Scandinavian grey wolf population, variation in MHC genes was compatible with expectations under neutrality, probably as a consequence of only three adults contributing to the re‐establishment of this population (Seddon & Ellegren ). Niskanen et al.…”

Section: Resultsmentioning

confidence: 99%

“…Niskanen et al. () found that grey wolves from Finland that were heterozygote for three MHC class II genes were less often infected by Trichinella spp., and carriers of specific MHC alleles, SNP haplotypes, and SNP alleles had fewer helminth infections, in what is a compelling example linking genetic variation with disease resistance. Another example of adaptive variation in grey wolves comes from the presence of a dominant allele in a beta‐defensin locus ( CBD103 or K locus), which makes the carrier of the allele black (Anderson et al.…”

Section: Resultsmentioning

confidence: 99%

Decades of population genetic research reveal the need for harmonization of molecular markers: the grey wolf Canis lupus as a case study

et al. 2015

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1.Following protection measures implemented since the 1970s, large carnivores are currently increasing in number and returning to areas from which they were absent for decades or even centuries. Monitoring programmes for these species rely extensively on non-invasive sampling and genotyping. However, attempts to connect results of such studies at larger spatial or temporal scales often suffer from the incompatibility of genetic markers implemented by researchers in different laboratories. This is particularly critical for long-distance dispersers, revealing the need for harmonized monitoring schemes that would enable the understanding of gene flow and dispersal dynamics. 2. Based on a review of genetic studies on grey wolves Canis lupus from Europe, we provide an overview of the genetic markers currently in use, and identify opportunities and hurdles for studies based on continent-scale datasets. 3. Our results highlight an urgent need for harmonization of methods to enable transnational research based on data that have already been collected, and to allow these data to be linked to material collected in the future. We suggest timely standardization of newly developed genotyping approaches, and propose that action is directed towards the establishment of shared single nucleotide polymorphism panels, next-generation sequencing of microsatellites, a common reference sample collection and an online database for data exchange. 4. Enhanced cooperation among genetic researchers dealing with large carnivores in consortia would facilitate streamlining of methods, their faster and wider adoption, and production of results at the large spatial scales that ultimately matter for the conservation of these charismatic species.

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“…The distance between DLA-DRB1 and DLA-DQA1 is 56.6 kb, while the distance between DLA-DQA1 and DLA-DQB1 is 77.7 kb. A previously established protocol [13] was used to sequence the loci in a cohort of 253 dogs. In addition, data from 41 families with 192 puppies from an earlier study by Kennedy et al [34] plus a further 12 families with 64 puppies from Rowan [35] were included.…”

Section: Methodsmentioning

confidence: 99%

“…MHC diversity differs from breed to breed and is often low [12], probably due to drift effects in small populations. However, even without free mate choice, MHC diversity in a dog breed can be close to the diversity of a wild wolf population [13, 14]. Humans have had major impact in some of the aspects that may influence the dog MHC diversity, for instance, through veterinary care and mate choice.…”

Section: Introductionmentioning

confidence: 99%

No evidence of prenatal diversifying selection at locus or supertype levels in the dog MHC class II loci

Niskanen

Kennedy

Lohi

et al. 2016

Canine Genet Epidemiol

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BackgroundDespite decades of studying, the mechanisms maintaining high diversity in the genes of the Major Histocompatibility Complex (MHC) are still puzzling scientists. In addition to pathogen recognition and other functions, MHC molecules may act prenatally in mate choice and in maternal-foetal interactions. These interactions are potential selective mechanisms that increase genetic diversity in the MHC. During pregnancy, immune response has a dual role: the foetus represents foreign tissue compared to mother, but histo-incompatibility is required for successful pregnancy. We have studied the prenatal selection in MHC class II loci (DLA-DQA1, DLA-DQB1 and DLA-DRB1) in domestic dogs by comparing the observed and expected offspring genotype proportions in 110 dog families. Several potential selection targets were addressed, including the peptide-binding site, the MHC locus, three-locus haplotype and supertype levels. For the supertype analysis, the first canine supertype classification was created based on in silico analysis of peptide-binding amino-acid polymorphism.ResultsIn most loci and levels, no deviation from the expected genotype frequencies was observed. However, one peptide-binding site in DLA-DRB1 had an excess of heterozygotes among the offspring. In addition, if the father shared a DLA-DRB1 allele with the mother, that allele was inherited by the offspring more frequently than expected, suggesting the selective advantage of a histo-compatible foetus, in contrast to our expectations.ConclusionsWe conclude that there is some evidence of post-copulatory selection at nucleotide site level in the MHC loci of pet dogs. But due to no indication of selection at locus, three-locus, or supertype levels, we estimated that the prenatal selection coefficient is less than 0.3 in domestic dogs and very likely other factors are more important in maintaining the genetic diversity in MHC loci.Electronic supplementary materialThe online version of this article (doi:10.1186/s40575-016-0038-9) contains supplementary material, which is available to authorized users.

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Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population

Cited by 55 publications

References 85 publications

Population genetic inferences using immune gene SNPs mirror patterns inferred by microsatellites

Population genetic inferences using immune gene SNPs mirror patterns inferred by microsatellites

Decades of population genetic research reveal the need for harmonization of molecular markers: the grey wolf Canis lupus as a case study

No evidence of prenatal diversifying selection at locus or supertype levels in the dog MHC class II loci

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